Lead (Pb2+) affects neuronal and endocrine systems that influence social interactions. By providing potential hiding locations, spatial heterogeneity may affect Pb2+-induced behavioral outcomes. Therefore, a test chamber was designed into which a refuge could be inserted. The refuge allowed test subjects to escape from the mirror image that stimulated agonistic interactions. Behaviors with a mirror were compared with baseline activity patterns without a mirror. Adult (12-month old) male and female zebrafish, exposed to Pb2+ (0–10 μM) as embryos (2–24 hours post fertilization), were tested individually for 5 min in each chamber design within 2 h of feeding. Behaviors were evaluated for % time in mirror zone, distance traveled (=activity level), and attacks on the mirror image. When there was no refuge, significant concentration-dependent increases occurred in male % time in mirror zone, activity level, and number of attacks. Increases in these variables were less pronounced in females. When there was a refuge, there were significant differences for males only in activity level and attacks at the higher developmental exposure concentrations; % time in mirror zone followed a similar pattern and level as without refuge. Females displayed Pb2+-induced behavioral changes only for attacks on mirror. Since the presence of refuges that is, environmental enrichment, reduced Pb2+-induced agonistic behavior in both sexes, experimental spatial design can be considered an important factor when interpreting behavioral outcomes.
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References
1.
BellingerDC. The protean toxicities of lead: new chapters in a familiar story. Int J Environ Res Public Health, 2011; 8:2593–2628.
2.
PokrasMA, KneelandMR. Lead poisoning: using transdisciplinary approaches to solve an ancient problem. Ecohealth, 2008; 5:379–385.
3.
RiceC, GhoraiJK, ZalewskiK, WeberDN. Developmental lead exposure causes startle response deficits in zebrafish. Aquat Toxicol, 2011; 105:600–608.
4.
ChenSS, LinCH, ChenTJ. Lead-induced attenuation in the aggregation of acetylcholine receptors during the neuromuscular junction formation. Toxicol Lett, 2005; 159:89–99.
5.
WalkowiakJ, AltmannL, KrämerU, SveinssonK, TurfeldM, Weishoff-HoubenMet al.Cognitive and sensorimotor functions in 6-year-old children in relation to lead and mercury levels: adjustment for intelligence and contrast sensitivity in computerized testing. Neurotoxicol Teratol, 1998; 20:511–521.
6.
OttoDA, FoxDA. Auditory and visual dysfunction following lead exposure. Neurotoxicology, 1993; 14:191–207.
7.
JuskoTA, HendersonCR, LanphearBP, Cory-SlechtaDA, ParsonsPJ, CanfieldRL. Blood lead concentrations<10 μg/dL and child intelligence at 6 years of age. Environ Health Perspect, 2008; 116:243–248.
8.
HaiderS, ShameemS, AhmedSP, PerveenT, HaleemDJ. Repeated administration of lead decreases brain 5-HT metabolism and produces memory deficits in rats. Cell Mol Biol Lett, 2005; 10:669–676.
9.
GuilarteTR, ToscanoCD, McGlothanJL, WeaverSA. Environmental enrichment reverses cognitive and molecular deficits induced by developmental lead exposure. Ann Neurol, 2003; 53:50–56.
10.
CervantesMC, DavidJT, LoydDR, SalinasJA, DelvilleY. Lead exposure alters the development of agonistic behavior in golden hamsters. Dev Psychobiol, 2005; 47:158–165.
11.
SlomanKA, BakerDW, HoCG, McDonaldDG, WoodCM. The effects of trace metal exposure on agonistic encounters in juvenile rainbow trout, Oncorhynchus mykiss. Aquat Toxicol, 2003; 63:187–196.
12.
BatainehH, Al-HamoodMH, ElbetiehaAM. Assessment of aggression, sexual behavior and fertility in adult male rat following long-term ingestion of four industrial metals salts. Hum Exp Toxicol, 1998; 17:570–576.
13.
DonaldJM, CutlerMG, MooreMR. Effects of lead in the laboratory mouse. Development and social behaviour after lifelong exposure to 12 μM lead in drinking fluid. Neuropharmacology, 1987; 26:391–399.
14.
HollowayWRJr, ThorDH. Low level lead exposure during lactation increases rough and tumble play fighting of juvenile rats. Neurotoxicol Teratol, 1987; 9:51–57.
15.
EngellennerWJ, BurrightRG, DonovickPJ. Lead, age and aggression in male mice. Physiol Behav, 1986; 36:823–828.
16.
CutlerMG. Effects of exposure to lead on social behaviour in the laboratory mouse. Psychopharmacology (Berlin), 1977; 52:279–282.
17.
MüllerYM, RiveroLB, CarvalhoMC, KobusK, FarinaM, NazariEM. Behavioral impairments related to lead-induced developmental neurotoxicity in chicks. Arch Toxicol, 2008; 82:445–451.
18.
DelvilleY. Exposure to lead during development alters aggressive behavior in golden hamsters. Neurotoxicol Teratol, 1999; 21:445–449.
19.
SoeiroAC, GouvêaTS, MoreiraEG. Behavioral effects induced by subchronic exposure to Pb and their reversion are concentration and gender dependent. Hum Exp Toxicol, 2007; 26:733–739.
20.
WeberDN, DingelWM, PanosJJ, StenpreisRE. Alterations in neurobehavioral responses in fishes exposed to lead and lead-chelating agents. Amer Zool, 1997; 37:354–362.
21.
WeberDN. Exposure to sublethal levels of waterborne lead alters reproductive behavior patterns in fathead minnows (Pimephales promelas)Neurotoxicology, 1993; 14:347–358.
22.
DolinskyZS, BurrightRG, DonovickPJ. Behavioral changes in mice following lead administration during several stages of development. Physiol Behav, 1983; 30:583–589.
23.
WangXM, LiuWJ, ZhangR, ZhouYK. Effects of exposure to low-level lead on spatial learning and memory and the expression of mGluR1, NMDA receptor in different developmental stages of rats. Toxicol Ind Health, 2012[Epub ahead of print]10.1177/0748233712436641.
24.
van WijngaardenE, WintersPC, Cory-SlechtaDA. Blood lead levels in relation to cognitive function in older U.S. adults. Neurotoxicology, 2011; 32:110–115.
BellingerDC. Very low lead exposures and children's neurodevelopment. Curr Opin Pediatr, 2008; 20:172–177.
27.
ChangW, ChenJ, WeiQY, ChenXM. Effects of Brn-3a protein and RNA expression in rat brain following low-level lead exposure during development on spatial learning and memory. Toxicol Lett, 2006; 164:63–70.
28.
NiheiMK, GuilarteTR. NMDAR-2A subunit protein expression is reduced in the hippocampus of rats exposed to Pb2+ during development. Brain Res Mol Brain Res, 1999; 66:42–49.
29.
GatewoodJD, WillsA, ShettyS, XuJ, ArnoldAP, BurgoynePSet al.Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. J Neurosci, 2006; 26:2335–2342.
30.
Lovell-BadgeR. Aggressive behaviour: contributions from genes on the Y chromosome. Novartis Found Symp, 2005; 268:20–33; discussion 33–41, 96–99.
31.
FrancisRC, BarlowGW. Social control of primary sex differentiation in the Midas cichlid. Proc Natl Acad Sci U S A, 1993; 90:10673–10675.
32.
CaoX, HuangS, RuanD. Enriched environment restores impaired hippocampal long-term potentiation and water maze performance induced by developmental lead exposure in rats. Dev Psychobiol, 2008; 50:307–313.
33.
DijkstraPD, SchaafsmaSM, HofmannHA, GroothuisTG. ‘Winner effect’ without winning: unresolved social conflicts increase the probability of winning a subsequent contest in a cichlid fish. Physiol Behav, 2012; 105:489–492.
34.
ArchardGA, BraithwaiteVA. Variation in aggressive behaviour in the poeciliid fish Brachyrhaphis episcopi: population and sex differences. Behav Processes, 2011; 86:52–57.
35.
TakeuchiY, HoriM, MyintO, KohdaM. Lateral bias of agonistic responses to mirror images and morphological asymmetry in the Siamese fighting fish (Betta splendens)Behav Brain Res, 2010; 208:106–111.
36.
HenryL, Le CarsK, MathelierM, BrudererC, HausbergerM. The use of a mirror as a ‘social substitute’ in laboratory birds. C R Biol, 2008; 331:526–531.
37.
LambertyY. The mirror chamber test for testing anxiolytics: is there a mirror-induced stimulation?Physiol Behav, 1998; 64:703–705.
38.
BronsteinPM. Socially mediated learning in male Betta splendens. J Comp Psychol, 1986; 100:279–284.
39.
AndersonJR. Responses to mirror image stimulation and assessment of self-recognition in mirror- and peer-reared stumptail macaques. Q J Exp Psychol B, 1983; 35:201–212.
40.
BernroiderG, PankseppJ. Mirrors and feelings: have you seen the actors outside?Neurosci Biobehav Rev, 2011; 35:2009–2016.
41.
VerityMA. Comparative observations on inorganic and organic lead neurotoxicity. Environ Health Perspect, 1990; 89:43–48.
42.
CarvanMJIII, LoucksE, WeberDN, WilliamsDE. Ethanol effects on the developing zebrafish: neurobehavior and skeletal morphogenesis. Neurotoxicol Teratol, 2004; 26:757–768.
43.
WeberDN, SpielerRE. Behavioral mechanisms of metal toxicity in fishes. In Aquatic Toxicology: Molecular, Biochemical, and Cellular Perspectives. MalinsDC, OstranderGK. Boca Raton, FL: Lewis Publishers, 1994; 421–467.
44.
Kasten-JollyJ, PabelloN, BolivarVJ, LawrenceDA. Developmental lead effects on behavior and brain gene expression in male and female BALB/cAnNTac mice. Neurotoxicology, 2012; 33:1005–1020.
45.
MielkeHW, ZahranS. The urban rise and fall of air lead (Pb) and the latent surge and retreat of societal violence. Environ Int, 2012; 43:48–55.
46.
BarretoRE, CarvalhoGG, VolpatoGL. The aggressive behavior of Nile tilapia introduced into novel environments with variation in enrichment. Zoology (Jena), 2011; 114:53–57.
47.
AlonsoF, HonjiRM, Guimarães MoreiraR, PandolfiM. Dominance hierarchies and social status ascent opportunity: anticipatory behavioral and physiological adjustments in a Neotropical cichlid fish. Physiol Behav, 2012; 106:612–618.
48.
DahlbomSJ, LagmanD, Lundstedt-EnkelK, SundströmLF, WinbergS. Boldness predicts social status in zebrafish (Danio rerio)PLoS One, 2011; 6:e23565.
49.
FilbyAL, PaullGC, BartlettEJ, Van LookKJ, TylerCR. Physiological and health consequences of social status in zebrafish (Danio rerio)Physiol Behav, 2010; 101:576–587.
50.
HenryMG, AtchisonGJ. Influence of social rank on the behavior of bluegill, Lepomis macrochirus Rafinesque, exposed to sublethal concentrations of cadmium and zinc. J Fish Biol, 1979; 15:309–315.
51.
RadilováJ, KovacevićN, RakićL, RadilT. Circadian differences in aggressive behavior of sea fish Serranus scriba. Homeost Health Dis, 1991; 33:155–156.
52.
WeberDN, SpielerRE. Effects of the light-dark cycle and scheduled feeding on behavioral and reproductive rhythms of the cyprinodont fish, Medaka, Oryzias latipes. Experientia, 1987; 43:621–624.
53.
HoyerPB. Damage to ovarian development and function. Cell Tissue Res, 2005; 322:99–106.
54.
ManireCA, RasmussenLE, GelsleichterJ, HessDL. Maternal serum and yolk hormone concentrations in the placental viviparous bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol, 2004; 136:241–247.
55.
AttekeC, VetillardA, FostierA, GarnierDH, JegoP, BailhacheT. Effects of progesterone and estradiol on the reproductive axis in immature diploid and triploid rainbow trout. Comp Biochem Physiol A Mol Integr Physiol, 2003; 134:693–705.
56.
NomuraM, DurbakL, ChanJ, SmithiesO, GustafssonJA, KorachKSet al.Genotype/age interactions on aggressive behavior in gonadally intact estrogen receptor beta knowckout (betaERKO) male mice. Horm Behav, 2002; 41:288–296.
57.
TaupeauC, PouponJ, TretonD, BrosseA, RichardY, MachelonV. Lead reduces messenger RNA and protein levels of cytochrome p450 aromatase and estrogen receptor beta in human ovarian granulosa cells. Biol Reprod, 2003; 68:1982–1988.
