Multiple environmental stressors elicit complex interactive effects in the western fence lizard (Sceloporus occidentalis)
Tóm tắt
Evaluation of multiple-stressor effects stemming from habitat degradation, climate change, and exposure to chemical contaminants is crucial for addressing challenges to ecological and environmental health. To assess the effects of multiple stressors in an understudied taxon, the western fence lizard (Sceloporus occidentalis) was used to characterize the individual and combined effects of food limitation, exposure to the munitions constituent 2,4,6-trinitrotoluene (TNT), and Plasmodium mexicanum (lizard malaria) infection. Three experimental assays were conducted including: Experiment I—TNT × Food Limitation, Experiment II—Food Limitation × Malaria Infection, and Experiment III—TNT × Malaria Infection. All experiments had a 30 day duration, the malaria treatment included infected and non infected control lizards, food limitation treatments included an ad libitum control and at least one reduced food ration and TNT exposures consisting of daily oral doses of corn oil control or a corn oil-TNT suspension at 5, 10, 20, 40 mg/kg/day. The individual stressors caused a variety of effects including: reduced feeding, reduced testes mass, anemia, increased white blood cell (WBC) concentrations and increased mass of liver, kidney and spleen in TNT exposures; reduced cholesterol, WBC concentrations and whole body, testes and inguinal fat weights given food limitation; and increased WBC concentrations and spleen weights as well as decreased cholesterol and testes mass in malaria infected lizards. Additive and interactive effects were found among certain stressor combinations including elimination of TNT-induced hormesis for growth under food limitation. Ultimately, our study indicates the potential for effects modulation when environmental stressors are combined.
Tài liệu tham khảo
Aiello FB, Keller JR, Klarmann KD, Dranoff G, Mazzucchelli R, Durum SK (2007) IL-7 induces myelopoiesis and erythropoiesis. J Immunol 178:1553–1563
Amo L, Lopez P, Martin J (2007) Habitat deterioration affects antipredatory behavior, body condition, and parasite load of female Psammodfrmus algirus lizards. Can J Zool 85:743–751
ATSDR (Agency for Toxic Substances and Disease Registry) (1995) Toxicological profile for TNT. U.S. Department of Health and Human Services, Atlanta, GA
Ayala SC (1970) Lizard malaria in California: description of a strain of Plasmodium mexicanum and biogeography of lizard malaria in western North America. J Parasitol 56:417–425
Bishop RW, Hable MA, Oliver CG, Valis RJ (2003) The USACHPPM gas chromatographic procedures for the analysis of waters and soils for energetics and related compounds. J Chromatogr 41:73–79
Cooper EL, Kempau AE, Zapate AG (1985) Reptilian immunity. In: Gans C, Billet F, Maderson PFA (eds) Biology of the reptilia. Wiley, New York, pp 599–678
Deng Y, Meyer SA, Guan X, Escalon BL, Ai J, Wilbanks MS, Welti R, Garcia-Reyero N, Perkins EJ (2011) Analysis of common and specific mechanisms of liver function affected by nitrotoluene compounds. PLoS ONE 6(2):e14662. doi:10.1371/journal.pone.0014662
Dilley JV, Tyson CA, Spanggord RJ, Sasmore DP, Newell GW, Dacre JC (1982) Short-term oral toxicity of 2,4,6-trinitrotoluene in mice, rats, and dogs. J Toxicol Environ Health 9:565–585
Dunlap KD, Schall JJ (1995) Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum. Physiol Zool 68:608–621
DuRant SE, Hopkins WA, Talent LG (2007) Energy acquisition and allocation in an ectothermic predator exposed to a common environmental stressor. Comp Biochem Phys C 145:442–448
Escalante A, Ayala FJ (1994) Phylogeny of the malarial genus Plasmodium, derived from rRNA gene sequences. Proc Natl Acad Sci USA 91:11373–11377
Foufopoulos J (1999) Host-parasite interactions in the mountain spiny lizard, Sceloporus jarrovi. Dissertation, University of Wisconsin-Madison
Frye FL (1991) Biomedical and surgical aspects of captive reptile husbandry. Krieger Publishing Company, FL
Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S, Winne CT (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50:653–666
Gogal RM, Johnson MS, Larsen CT, Prater MR, Duncan RB, Ward DL, Holladay SD (2002) Influence of dietary 2,4,6-trinitrotoluene (TNT) exposure in the northern bobwhite (Colinus virginianus). Environ Toxicol Chem 21:81–86
Guillette LJ Jr, Casas-Andreu G (1981) Seasonal variation in fat body weights of the Mexican high elevation lizard Sceloporus grammicus microlepidotus. J Herp 15(3):366–371
Holem RR, Hopkins WA, Talent LG (2006) Effect of acute exposure to malathion and lead on sprint performance of the western fence lizard (Sceloporus occidentalis). Arch Environ Contam Toxicol 51:111–116
Homma-Takeda S, Hiraku Y, Ohkuma Y, Oikawa S, Murata M, Ogawa K, Iwamuro T, Li S, Sun GF, Kumagai Y, Shimojo N, Kawanishi S (2002) 2,4,6-trinitrotoluene-induced reproductive toxicity via oxidative DNA damage by its metabolite. Free Radic Res 36:555–566
IPCC (Intergovernmental Panel on Climate Change) (2007) The physical science basis. Cambridge University Press, New York
Johnson MS, Quinn MJ, Bazar MA, Gust KA, Escalon BL, Perkins EJ (2007) Subacute toxicity of oral 2,6-dinitrotoluene and 1,3,5-trinitro-1,3,5-triazine (RDX) exposure to the northern bobwhite. Environ Toxicol Chem 26(7):1481–1487
Kaiser J (2003) Hormesis: sipping from a poisoned chalice. Science 302:376–379
Keller JM, McClellan-Green PD, Lee AM, Arendt MD, Maier PP, Segars AL, Whitaker JD, Keil DE, Peden-Adams MM (2005) Mitogen-induced lymphocyte proliferation in loggerhead sea turtles: comparison of methods and effects of gender, plasma testosterone concentration, and body condition on immunity. Vet Immunol Immunop 103:269–281
Leung KH, Yao M, Stearns R, Chiu S-HL (1995) Mechanism of bioactivation and covalent binding of 2,4,6-trinitrotoluene. Chem Biol Interact 97:37–51
Levine BS, Furedi EM, Gordon DE, Lish PM, Barkley JJ (1984) Subchronic toxicity of trinitrotoluene in Fisher 344 rats. Toxicology 32:253–265
Levine BS, Rust JS, Barkley JJ, Furedi EM, Lish PM (1990) Six-month oral toxicity study of trinitrotoluene in beagle dogs. Toxicology 63:233–244
McCormick NG, Feeherry FE, Levinson HS (1976) Microbial transformation of 2,4,6-trinitrotoluene and other nitroaromatic compounds. Appl Environ Microb 31:949–958
McFarland CA, Quinn MJ Jr, Bazar MA, Remick AK, Talent LG, Johnson MS (2008) Toxicity of oral exposure to 2,4,6-trinitrotoluene in the western fence lizard (Sceloporus occidentalis). Environ Toxicol Chem 27:1102–1111
McFarland CA, Quinn MJ Jr, Bazar MA, Talent LG, Johnson MS (2009) Toxic effects of oral hexahydro-1,3,5-trinitro-1,3,5-triazine in the western fence lizard (Sceloporus occidentalis). Environ Toxicol Chem 28:1043–1050
McFarland CA, Quinn MJ Jr, Bazar MA, Talent LG, Johnson MS (2011) Toxic effects of oral 2-amino-4,6-dinitrotoluene in the western fence lizard (Sceloporus occidentalis). Environ Pollut 159:446–473
Munns WR Jr (2006) Assessing risks to wildlife populations from multiple stressors: overview of the problem and research needs. Ecol Soc 11(1):23–34
Neal AT, Schall JJ (2010) Gametocyte sex ratio in single-clone infections of the malaria parasite Plasmodium mexicanum. Parasitology 137:1851–1859
Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: environmental contaminants in a warming world. Environ Int 35(6):971–986
Osgood SM, Schall JJ (2004) Gametocyte sex ratio of a malaria parasite: response to experimental manipulation of parasite clonal diversity. Parasitology 128:23–29
Paul REL, Brey PT (2003) Malaria parasites and red blood cells: from anemia to transmission. Mol Cells 15:139–149
Rawat A, Gust KA, Deng Y, Garcia-Reyero N, Quinn Jr MJ, Johnson MS, Indest K, Elasri MO, Perkins EJ (2010) From raw materials to validated system: the construction of genomic library and microarray to interpret systemic perturbation in Northern Bobwhite. Physiol Genom 42:219–235
Reddy G, Chandra SAM, Lish JW, Qualls CW Jr (2000) Toxicity of 2,4,6-trinitrotoluene (TNT) in hispid cotton rats (Sigmodon hispidus): hematological, biochemical, and pathological effects. Int J Toxicol 19:169–177
Rocheleaua S, Kuperman RG, Martel M, Paquet L, Bardaia G, Wong S, Sarrazina M, Dodard S, Gong P, Hawaria J, Checkai JT, Sunaharaa GI (2006) Phytotoxicity of nitroaromatic energetic compounds freshly amended or weathered and aged in sandy loam soil. Chemosphere 62:545–558
Schall JJ (1990) Virulence of lizard malaria: the evolutionary ecology of an ancient parasite-host association. Parasitology 100:S35–S52
Schall JJ (1996) Malarial parasites of lizards: diversity and ecology. Adv Parasit 37:255–333
Schall JJ, Dearing MD (1987) Malarial parasitism and male competition for mates in the western fence lizard, Sceloporus occidentalis. Oecologia 73:389–392
Schall JJ, Marghoob AB (1995) Prevalence of a malarial parasite over time and space: Plasmodium mexicanum in its vertebrate host, the western fence lizard, Sceloporus occidentaliis. J Anim Ecol 64:177–185
Schall JJ, Bennett AF, Putnam RW (1982) Lizards infected with malaria: physiological and behavioral consequences. Science 217:1057–1059
Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, Lara-Resendiz R, Martínez-Méndez N, Calderón-Espinosa ML, Meza-Lázaro RN, Gadsden H, Avila LJ, Morando M, De la Riva IJ, Sepulveda PV, Rocha CFD, Ibargüengoytía N, Puntriano CA, Massot M, Lepetz V, Oksanen TA, Chapple DG, Bauer AM, Branch WR, Clobert J, Sites JW Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894–899
Spain JC (1995) Biodegradation of nitroaromatic compounds. Annu Rev Microbiol 49:523–555
Steevens JA, Duke BM, Lotufo GR, Bridges TS (2002) Toxicity of the explosives 2,4,6-trinitrotoluene, hexahydro-1,3,5-trinitro-1,3,5-triazine, and octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine in sediments to Chironomus tentans and Hyalella azteca: low-dose hormesis and high-dose mortality. Environ Toxicol Chem 21(7):1475–1482
Sykes JM, Klaphake E (2008) Reptile hematology. In: Veterinary clinics of North America exotic animal practice. WB Saunders, Philadelphia, pp 481–500
Talent LG, Dumont JN, Bantle JA, Janz DM, Talent SG (2002) Evaluation of western fence lizards (Sceloporus occidentalis) and eastern fence lizards (Sceloporus undulatus) as laboratory reptile models for toxicological investigations. Environ Toxicol Chem 21:899–905
Tavares-Dias M, Oliveira-Junior AA, Silva MG, Marcon JL, Barcellos JFM (2009) Comparative hematological and biochemical analysis of giant turtles from the Amazon farmed in poor and normal nutritional conditions. Vet Arhiv 79(6):601–610
Vardo-Zalik AM, Schall JJ (2008) Clonal diversity within infections and the virulence of a malaria parasite, Plasmodium mexicanum. Parasitology 135:1363–1372
Yinon J (1990) Toxicity and metabolism of explosives. CRC Press, Boca Raton
Yotoko KSC, Elisei C (2006) Malaria parasites (Apicomplexa, Haematozoea) and their relationships with their hosts: is there an evolutionary cost for the specialization? J Zool Syst Evol Res 44(4):265–273