ArticlePDF Available

The effect of artificial light on male breeding-season behaviour in green frogs, Rana clamitans melanota

Authors:

Abstract

Artificial night lighting (or ecological light pollution) is only now gaining attention as a source of long-term effects on the ecology of both diurnal and nocturnal animals. The limited data available clearly indicate that artificial light can affect physiology and behaviour of animals, leading to ecological consequences at the population, community, and ecosystem levels. Aquatic ecosystems may be particularly vulnerable to such effects, and nocturnally breeding animals such as frogs may be especially affected. To address this potential, we quantify the effects of artificial light on calling and movement behaviour in a rural population of male green frogs (Rana clamitans melanota (Rafinesque, 1820)) during the breeding season. When exposed to artificial light, frogs produced fewer advertisement calls and moved more frequently than under ambient light conditions. Results clearly demonstrate that male green frog behaviour is affected by the presence of artificial light in a manner that has the potential to reduce recruitment rates and thus affect population dynamics.
NOTE / NOTE
The effect of artificial light on male breeding-
season behaviour in green frogs, Rana clamitans
melanota
B.J. Baker and J.M.L. Richardson
Abstract: Artificial night lighting (or ecological light pollution) is only now gaining attention as a source of long-term ef-
fects on the ecology of both diurnal and nocturnal animals. The limited data available clearly indicate that artificial light
can affect physiology and behaviour of animals, leading to ecological consequences at the population, community, and
ecosystem levels. Aquatic ecosystems may be particularly vulnerable to such effects, and nocturnally breeding animals
such as frogs may be especially affected. To address this potential, we quantify the effects of artificial light on calling and
movement behaviour in a rural population of male green frogs (Rana clamitans melanota (Rafinesque, 1820)) during the
breeding season. When exposed to artificial light, frogs produced fewer advertisement calls and moved more frequently
than under ambient light conditions. Results clearly demonstrate that male green frog behaviour is affected by the presence
of artificial light in a manner that has the potential to reduce recruitment rates and thus affect population dynamics.
Re
´sume
´:L’e
´clairement artificiel de nuit (la pollution lumineuse e
´cologique) commence tout juste a
`e
ˆtre reconnue comme
une source d’effets a
`long terme sur l’e
´cologie tant des animaux diurnes que nocturnes. Les rares donne
´es disponibles indi-
quent clairement que la lumie
`re artificielle peut affecter la physiologie et le comportement des animaux, avec des conse
´-
quences sur l’e
´cologie de la population, de la communaute
´et de l’e
´cosyste
`me. Les e
´cosyste
`mes aquatiques pourraient e
ˆtre
particulie
`rement vulne
´rables a
`ces effets, surtout les animaux a
`reproduction nocturne comme les grenouilles. Afin de ve
´ri-
fier ces conse
´quences potentielles, nous mesurons les effets de la lumie
`re artificielle sur les comportements d’appel et de
de
´placement chez une population rurale de grenouilles vertes (Rana clamitans melanota (Rafinesque, 1820)) ma
ˆles durant
la saison de reproduction. Expose
´es a
`la lumie
`re artificielle, les grenouilles e
´mettent moins d’appels de signalisation et se
de
´placent plus fre
´quemment que sous un re
´gime de lumie
`re ambiante. Ces re
´sultats de
´montrent clairement que le com-
portement des grenouilles vertes ma
ˆles est affecte
´par la pre
´sence de lumie
`re artificielle d’une fac¸on qui pourrait re
´duire
les taux de recrutement et ainsi affecter la dynamique de la population.
[Traduit par la Re
´daction]
Introduction
While nocturnal animals experience natural variance in
light levels through changes in moon phase and cloud cover,
artificial lights are typically brighter and less diffuse than
moonlight illumination, generating very different patterns of
light change. A recently published collection of papers from
the first North American conference on the ecological ef-
fects of artificial night lighting clearly indicates both the
enormous potential for large effects of artificial light on all
taxa and the dearth of data regarding the consequences of
these anthropogenic habitat changes (Rich and Longcore
2006). Aquatic ecosystems in particular can be especially
sensitive to the effects of ecological light pollution (Rich
and Longcore 2006). The purpose of this study is to quantify
the effects of change in light environment on the breeding-
season behaviour of male green frogs, Rana clamitans mela-
nota (Rafinesque, 1820).
While astronomers began sounding an alarm regarding
light pollution 30 years ago (Berry 1976), little has been
done to quell the problem (Tyson 2002). Zoologists have
only recently begun to consider the potential effect of artifi-
cial lights on nocturnal animals (Rich and Longcore 2006).
Two aspects of artificial lighting may have important and
different consequences on animal populations: chronic in-
creases in mean light level and increased variation in light
level created by spot lighting (Buchanan 2006). Recent liter-
ature suggests that both nocturnal and diurnal animals can
Received 1 March 2006. Accepted 28 August 2006. Published on the NRC Research Press Web site at http://cjz.nrc.ca on 5 December
2006.
B.J. Baker and J.M.L. Richardson.1Department of Biological Sciences, 500 Glenridge Avenue, Brock University, St. Catharines, ON
L2S 3A1, Canada.
1Corresponding author (e-mail: jrichardson@brocku.ca).
1528
Can. J. Zool. 84: 1528–1532 (2006) doi:10.1139/Z06-142 #2006 NRC Canada
be affected by artificial lighting. For example, sea turtle
hatchlings are disoriented by artificial street lighting near
beaches (Tuxbury and Salmon 2005). Beach mice reduce
foraging in the presence of artificial lighting (Bird et al.
2004). Conversely, many insectivorous frogs, bats, and birds
take advantage of streetlamps for the large aggregation of
insects they typically attract, thereby increasing foraging
success rates (Buchanan 2006; Longcore and Rich 2006;
Rydell 2006). Robins, diurnal in nature, begin their dawn
chorus earlier in sites that have increased night lighting,
starting their chorus during true night in highly lit areas,
with no apparent relationship to actual sunrise (Miller 2006).
Anurans may be especially vulnerable to effects of artifi-
cial lighting. First, their nocturnal habits require dark-
adapted eyes, and a sudden increase of light not only dis-
rupts this but, depending on the brightness of the light, can
require a long recovery period before the eyes return to a
dark-adapted state (Cornell and Hailman 1984; Fain et al.
2001). Frogs are particularly likely to experience such dy-
namic light change because they tend to be in vegetated
areas where spotlights and vegetation are likely to co-occur,
creating a habitat that has extremes of light and dark within
a small area. Further, wind leads to movement of branches
that makes these light and dark areas unpredictable in loca-
tion. Another reason dynamic light change is likely to be
particularly relevant to frog populations is that frogs are
often in the proximity of roads (either when breeding in
ditches or when migrating to ponds across roads), and car
headlights create strong, sudden, and transient light level
changes.
Studies of the behaviour of nocturnal frogs have been fur-
ther complicated by the tendency for researchers to use
flashlights or headlamps to light their own way and to locate
animals. Several researchers have noted anecdotally that
frog calling seems unaffected by the use of a flashlight
(e.g., Martof 1953a, 1953b, 1956; Howard 1978), although
Howard (1978) also noted that his light disrupted mating in
bullfrogs (Rana catesbeiana Shaw, 1802). Further, many
frog species are known to respond to light in a variety of
ways (Jaeger and Hailman 1973). Light levels affect both
male calling behaviour and female mate choice behaviour
in Tu
´ngara frogs (Physalaemus pustulosus (Cope, 1864)), as
well as calling and anti-predator behaviour in the treefrog
Smilisca sila Duellman and Trueb, 1966 (Tuttle and Ryan
1982; Tuttle et al. 1982; Rand et al. 1997). Buchanan
(1998) studied the effects of artificial light use on foraging
behaviour of the gray treefrog (Hyla chrysoscelis Cope,
1880) and observed that rapid increases in light intensity
(such as those generated by use of headlamps or flashlights)
led to decreased foraging performance.
In this study, we quantify the effects of artificial light on
the behaviour of territorial male green frogs (R. clamitans)
in the field during the breeding season, when males call to
attract mates. Data were collected from a population of frogs
in a rural area to minimize the potential of confounding ur-
ban human disturbance effects (Longcore and Rich 2004).
We used a paired design to consider the change in calling
and movement behaviour of frogs under ambient light con-
ditions (observed with night vision goggles) compared with
artificial light conditions. The purpose of our study is to as-
sess the potential for ecological consequences of artificial
lighting on anuran populations by comparing male green
frog behaviour in the presence and absence of artificial light.
Methods
Rana clamitans males were observed in a swampy area
of Wainfleet Bog, Niagara Region, Ontario, Canada
(42853N, 79820W). The site had thick low brush inter-
spersed with areas of open water of depths ranging from
approximately 0.2 to 1 m. Observations were taken be-
tween 2000 and 0100 from 1 July 2003 to 4 August 2003.
Cloud cover conditions were noted during observations and
the effects of lunar phase and cloud cover were considered
in subsequent analyses. Frogs were located by calls and
without artificial light (the ‘ATN Viper’’ IR generation 1
night vision scope was used by the researcher to see).
Once a frog was located and the researcher was positioned
for observations (approximately 2 m away), frogs were
given a 5 min habituation period (under the appropriate
light treatment). Observations were then recorded for
15 min. A 5 min habituation period is long enough to al-
low the frog’s eyes to become mostly adapted to the artifi-
cial light (Fain et al. 1996; Calvert et al. 2002), although
subtle pupillary responses to light change are known to
continue for many hours (Cornell and Hailman 1984).
We used a paired design to test for the effect of light on
behaviour while controlling for differences among males.
Frogs were observed from the same position for each treat-
ment (the position was marked with flagging tape during the
first observation to allow the observer to find the same posi-
tion for the second observation) and frogs were left undis-
turbed for 1 h between observation periods, allowing frogs’
eyes to return to a dark-adapted state (Leibrock et al. 1994)
for those frogs that received the light treatment first. Treat-
ment order was arbitrarily assigned for each frog; 9 frogs re-
ceived the ambient light treatment first and 11 frogs
received the artificial light treatment first. The calling site
of each frog was mapped and each site was used only once
for each treatment. While it is possible that some males
switched sites during the 4 weeks of observations, R. clami-
tans males typically use the same calling site for extended
periods (Martof 1953b; Wells 1977), so the probability that
the same male was sampled more than once is low.
Light treatments
In the ambient light treatment, no artificial light was used
and frog behaviour was observed with the same night vision
goggles used to locate frogs initially. Frogs do not detect IR
light (Jaeger and Hailman 1973; Buchanan 1998).
The artificial white light treatment was created using a
Maglite1flashlight (3 D battery size). The flashlight was
used to illuminate the frog and a circular area with a diame-
ter of approximately 1 m surrounding the frog. Throughout
the trial the frog was kept in the centre of the light. Flash-
light batteries were replaced regularly and before noticeable
dimming of the flashlight occurred. Regrettably, we were
unable to measure actual light levels in the field for each
observation. However, we recreated the same beam width
and distance, in the laboratory, subsequent to this study. We
measured light energy output using an LI-189 Quantum/
Radiometer/Photometer (LI-COR Inc., Lincoln, Nebraska);
Baker and Richardson 1529
#2006 NRC Canada
output was 0.73 mmol/m2s–1 with 4-week-old batteries and
1.66 mmol/m2s–1 with new batteries. Standard conversion,
based on the predominant wavelength energy of visible
light (Sager and McFarlane 1997), leads us to estimate
that the light output we used ranged from approximately
52 lx to 120 lx.
Analyses
During each observation period, each call and movement
of the frog was recorded. Only type I advertisement calls
(Wells 1978) were observed; these calls typically consist of
a single note but can also be multi-note calls (Wells 1978;
Ramer et al. 1983). Multi-note calls were identified as dou-
ble, triple, or four-plus calls. A movement was defined as
movement of any body part, whether it resulted in displace-
ment of the male from its initial location or not. Movements
that resulted in any displacement were noted separately but
occurred too seldom to analyse separately.
Differences in mean numbers of calls and movements be-
tween artificial light and ambient light treatments were ana-
lysed using a repeated measures MANOVA, with light
treatment (artificial versus ambient light) as one repeated
measure and behaviour (movement versus calling) as a sec-
ond repeated measure. Independent factors included in the
model were moon (moonlit night versus no moon visible)
and treatment order (observations done in light first or sec-
ond). Both the number of calls and the number of move-
ments were log-transformed prior to analysis to meet
parametric assumptions. Number of calls was transformed
using ln(calls + 1) and number of movements was trans-
formed using ln(movements + 0.1), as movements occurred
at a frequency of roughly 10% of that of calls. The effect of
treatment on complex calls was further analysed separately
from single calls, using a Wilcoxon’s signed-ranks test be-
cause a high number of zeros in the artificial light data vio-
lated assumptions for a parametric test.
Results
Frogs observed under ambient light conditions called
more (total calls = 453 in ambient light versus 256 in artifi-
cial light) and moved less (total moves = 12 in ambient light
versus 81 in artificial light) (Wilks’ statistic = 0.337,
F[1,16] = 31.42, P= 0.001). A significant interaction was
also present between behaviour (calling versus movement)
and the artificial light treatment along with significant main
effects for behaviour and artificial light (Wilks’ statistic =
0.212, F[1,16] = 59.53, P= 0.001). The significant interaction
effect occurs because movement increases in the light, while
calling decreases (Fig. 1). No other interaction terms were
statistically significant. Notably, further consideration of
only the relatively rare complex calls shows strong treatment
effects. Double calls occurred 2.9 (±1.6) times, on average,
in ambient light compared with 0.15 (±0.109) times in artifi-
cial light (Wilcoxon’s signed-ranks test; P= 0.008). The tri-
ple and four-plus calls occurred only under ambient light
(3 times and 1 time, respectively).
Treatment order had no effect on calling or movement be-
haviour (repeated measures ANOVA; F[1,16] < 0.005, P>
0.99), nor did it interact with light effects (Wilks’ statistic =
0.21, F[1,16] = 0.13, P= 0.72). Six of the 20 frogs were
observed on nights that had both a full moon and a clear
sky (observations done 13, 14, and 16 July). The behaviour
of individuals tested on these nights did not differ from
that of the other 14 frogs (repeated measures ANOVA;
F[1,16] = 0.06, P= 0.81).
Discussion
Male green frogs modify behaviour in the presence of ar-
tificial light. In particular, frogs called less, performed fewer
multi-note calls, and moved more frequently in the presence
of artificial light. This is in contrast to previously published
anecdotes suggesting that light does not affect frog territorial
behaviour (Martof 1953a; Howard 1978), but in agreement
with more recent data suggesting that high levels of ambient
light may prevent frogs from chorusing (Buchanan 2006).
Many nocturnal animals modify activity and foraging
rates with changing light levels (moonlight or artificial light;
reviewed in Kronfeld-Schor and Dayan 2003). Moonlight
has long been known to affect frog reproductive physiology
and behaviour, either through changes in female receptivity
(Church 1960, 1961) or through changes in activity and
movement during the full moon (Ferguson 1960; Fitzgerald
and Bider 1974). Decreased calling with increased light may
also reflect an anti-predator response, similar to the de-
creased foraging of many nocturnal rodents during a full
moon to minimize predation risk (Kotler 1984; Wolfe and
Summerlin 1989; Topping et al. 1999; Kramer and Birney
2001).
0
2
4
6
8dark
light
Number of Moves
0
10
20
30
40
Number of Calls
Moon No Moon
Fig. 1. Calling and movement of Rana clamitans males on terri-
tories. Manipulated treatments were dark (no artificial light) and
light (flashlight-illuminated frog). All frogs (n= 20) were observed
under both treatments. Data are further divided by ambient light
conditions: moon = clear, moonlit night (n= 6); no moon = cloudy
or new-moon night (n= 14).
1530 Can. J. Zool. Vol. 84, 2006
#2006 NRC Canada
The results of this study reveal a potential for artificial
lighting to negatively affect breeding success, particularly
dynamic light changes such as those generated by car head-
lights, landscape lighting that is partially occluded by vege-
tation (leading to dark and light areas in close spatial
proximity, such that the frog moving a short distance may
encounter large differences in light level), or lighting that is
activated by a motion detector and then stays on for some
pre-set time period. The light stimulus in our study differed
somewhat from that predicted to come from cars, etc., as the
frog was exposed to the light stimulus for a 5 min acclima-
tion period prior to data collection. We suggest that our data
are conservative relative to higher frequency light changes
because the sudden onset of light leads quickly to desensiti-
zation of light receptors in the vertebrate eye, and the subse-
quent return to dark adaptation by the eye occurs far more
slowly (Fain et al. 2001). Further, frogs have a greatly re-
duced ability, compared with birds or mammals, to control
light levels reaching the retina through pupillary responses
(Cornell and Hailman 1984).
Individuals in this population were in an unlit rural loca-
tion, far from any houses, and we expect our results to re-
flect those of a population naı
¨ve to light effects. Further
work on whether populations adjust to static changes in light
levels remains to be done. Regardless of any chronic in-
crease in background light levels, dynamic changes in light
levels are still likely to occur. If such dynamic light reduces
the amount of time a frog is calling by even a small percent-
age, the effects on mating success may be large (depending
on the relationship between time spent calling and the prob-
ability of attracting a female) and hence may lead to a sig-
nificant decrease in population recruitment rates. This
potential is especially distressing given observed global am-
phibian declines.
Acknowledgements
Thanks to M.H. Richards for comments on multiple ver-
sions of this work. This research was funded by the Depart-
ment of Biological Sciences, Brock University and the
Natural Sciences and Engineering Research Council of Can-
ada (Discovery Grant No. 261587-03 to J.M.L.R.).
References
Berry, R.L. 1976. Light pollution in southern Ontario. J. R. Astr.
Soc. Can. 70: 97–115.
Bird, B.L., Branch, L.C., and Miller, D.L. 2004. Effects of coastal
lighting on foraging behavior of beach mice. Conserv. Biol. 18:
1435–1439. doi:10.1111/j.1523-1739.2004.00349.x.
Buchanan, B.W. 1998. Low-illumination prey detection by squirrel
treefrogs. J. Herpetol. 32: 270–274. doi:10.2307/1565308.
Buchanan, B.W. 2006. Observed and potential effects of artificial
night lighting on anuran amphibians. In Ecological conse-
quences of artificial night lighting. Edited by C. Rich and T.
Longcore. Island Press, Washington, D.C. pp. 192–220.
Calvert, P.D., Govardovskii, V.I., Arshavsky, V.Y., and Makino,
C.L. 2002. Two temporal phases of light adaptation in retinal
rods. J. Gen. Physiol. 119: 129–145. doi:10.1085/jgp.119.2.129.
PMID:11815664.
Church, G. 1960. The effects of seasonal and lunar changes on the
breeding pattern of the edible Javanese frog, Rana cancrivora
(Gravenhurst). Treubia, 25: 215–233.
Church, G. 1961. Seasonal and lunar variation in the numbers of
mating toads in Bandung (Java). Herpetologica, 17: 122–126.
Cornell, E.A., and Hailman, J.P. 1984. Pupillary responses of two
Rana pipiens-complex anuran species. Herpetologica, 40: 356–
366.
Fain, G.L., Matthews, H.R., and Cornwall, M.C. 1996. Dark adap-
tation in vertebrate photorecepters. Trends Neurosci. 19: 502–
507. doi:10.1016/S0166-2236(96)10056-4. PMID:8931277.
Fain, G.L., Matthews, H.R., Cornwall, M.C., and Koutalos, Y.
2001. Adaptation in vertebrate photoreceptors. Physiol. Rev. 81:
117–151. PMID:11152756.
Ferguson, D.E. 1960. Observations on movements and behavior of
Bufo fowleri in residential areas. Herpetologica, 16: 112–115.
Fitzgerald, G.J., and Bider, J.R. 1974. Influence of moon phase and
weather factors on locomotory activity in Bufo americanus. Oi-
kos, 25: 338–340.
Howard, R.D. 1978. Influence of male-defended oviposition sites
on early embryo mortality in bullfrogs. Ecology, 59: 789–798.
doi:10.2307/1938783.
Jaeger, R.G., and Hailman, J.P. 1973. Effects of intensity on the
phototactic responses of adult anuran amphibians: a comparative
survey. Z. Tierpsychol. 33: 352–407. PMID:4206432.
Kotler, B.P. 1984. Risk of predation and the structure of desert ro-
dent communities. Ecology, 65: 689–701. doi:10.2307/1938041.
Kramer, K.M., and Birney, E.C. 2001. Effect of light intensity on
activity patterns of patagonian leaf-eared mice, Phyllotis xantho-
pygus. J. Mammal. 82: 535–544. doi:10.1644/1545-1542(2001)
082<0535:EOLIOA>2.0.CO;2.
Kronfeld-Schor, N., and Dayan, T. 2003. Partitioning of time as an
ecological resource. Annu. Rev. Ecol. Syst. 34: 153–181.
Leibrock, C.S., Reuter, T., and Lamb, T.D. 1994. Dark adaptation
of toad rod receptors following small bleaches. Vision Res. 34:
2787–2800. doi:10.1016/0042-6989(94)90048-5. PMID:7975314.
Longcore, T., and Rich, C. 2004. Ecological light pollution. Front.
Ecol. Environ. 2: 191–198.
Longcore, T., and Rich, C. 2006. Synthesis. In Ecological conse-
quences of artificial night lighting. Edited by C. Rich and T.
Longcore. Island Press, Washington, D.C. pp. 413–430.
Martof, B. 1953a. Home range and movements of the green frog,
Rana clamitans. Ecology, 34: 529–543. doi:10.2307/1929725.
Martof, B. 1953b. Territoriality in the green frog, Rana clamitans.
Ecology, 34: 165–174. doi:10.2307/1930316.
Martof, B. 1956. Factors influencing size and composition of popu-
lations of Rana clamitans. Am. Midl. Nat. 56: 224–245. doi:10.
2307/2422457.
Miller, M.W. 2006. Apparent effects of light pollution on singing
behavior of American robins. Condor, 108: 130–139. doi:10.
1650/0010-5422(2006)108[0130:AEOLPO]2.0.CO;2.
Ramer, J.D., Jenssen, T.A., and Hurst, C.J. 1983. Size-related var-
iation in the advertisement call of Rana clamitans (Anura: Rani-
dae), and its effect on conspecific males. Copeia, 1983(1): 141–
155. doi:10.2307/1444708.
Rand, A.S., Bridarolli, M.E., Dries, L., and Ryan, M.J. 1997. Light
levels influence female choice in Tungara frogs: predation risk
assessment? Copeia, 1997(2): 447–450. doi:10.2307/1447770.
Rich, C., and Longcore, T. (Editors). 2006. Ecological consequences
of artificial night lighting. Island Press, Washington, D.C.
Rydell, J. 2006. Bats and their insect prey at streetlights. In Ecolo-
gical consequences of artificial night lighting. Edited by C. Rich
and T. Longcore. Island Press, Washington, D.C. pp. 43–60.
Sager, J.C., and McFarlane, J.C. 1997. Radiation. In Plant growth
chamber handbook. Edited by R.W. Langhans and T.W. Tib-
bitts. Iowa Agric. Home Econ. Exp. Stn. Spec. Rep. No. 99.
pp. 1–30.
Baker and Richardson 1531
#2006 NRC Canada
Topping, M.G., Millar, J.S., and Goddard, J.A. 1999. The effects of
moonlight on nocturnal activity in bushy-tailed wood rats (Neo-
toma cinerea). Can. J. Zool. 77: 480–485. doi:10.1139/cjz-77-3-
480.
Tuttle, M.D., and Ryan, M.J. 1982. The role of synchronized call-
ing, ambient light, and ambient noise, in anti-bat predator beha-
vior of a treefrog. Behav. Ecol. Sociobiol. 11: 125–131. doi:10.
1007/BF00300101.
Tuttle, M.D., Taft, L.K., and Ryan, M.J. 1982. Evasive behavior of
a frog in response to bat predation. Anim. Behav. 30: 393–397.
doi:10.1016/S0003-3472(82)80050-X.
Tuxbury, S.M., and Salmon, M. 2005. Competitive interactions be-
tween artificial lighting and natural cues during seafinding by
hatchling marine turtles. Biol. Conserv. 121: 311–316. doi:10.
1016/j.biocon.2004.04.022.
Tyson, N.D. 2002. Let there be dark. Nat. Hist. 111: 34–37.
Wells, K.D. 1977. Territoriality and male mating success in green
frog (Rana clamitans). Ecology, 58: 750–762. doi:10.2307/
1936211.
Wells, K.D. 1978. Territoriality in the green frog (Rana clamitans)—
vocalizations and agonistic behavior. Anim. Behav. 26: 1051–
1063. doi:10.1016/0003-3472(78)90094-5.
Wolfe, J.L., and Summerlin, C.T. 1989. The influence of lunar
light on nocturnal activity of the old-field mouse. Anim. Behav.
37: 410–414. doi:10.1016/0003-3472(89)90088-2.
1532 Can. J. Zool. Vol. 84, 2006
#2006 NRC Canada
... A total of 216 studies were identified. These studies included behavioral and physiological responses in plants [59][60][61][62][63][64][65][66][67][68][69][70][71][72][73][74][75][76][77]; arthropods, including insects and spiders [71,; fish ; amphibians [148][149][150][151][152][153][154][155][156][157][158][159]; reptiles [160][161][162][163][164][165][166][167]; birds ; and non-human mammals, including bats, primates, rodents, and marsupials [24,160,161,174,, when their habitats, aquatic or terrestrial, were artificially illuminated with direct or indirect emissions of ALAN (i.e., all light sources of artificial light). The results of our systematic review show that the most studied organism groups exposed to night-time illumination were birds (76 studies); arthropods, insects and spiders (43 studies); non-human mammals, including bats, primates, rodents, and marsupials (30 studies); fish (28 studies); plants (19 studies); amphibians (12 studies); and reptiles (8 studies). ...
... ALAN was reported to alter amphibian behavioral responses, including the preference for shelter [148]; attraction toward urban edges, which might lead to an altered passage choice of habitats typically visited [149,150]; altered vocalization calls [151,152]; altered detection and consumption of prey [153]; altered attempts to capture prey [154]; increased activity [155]; and mate selection and reproductive success [156]. ...
Article
Full-text available
The application of lighting technologies developed in the 20th century has increased the brightness and changed the spectral composition of nocturnal night-time habitats and night skies across urban, peri-urban, rural, and pristine landscapes, and subsequently, researchers have observed the disturbance of biological rhythms of flora and fauna. To reduce these impacts, it is essential to translate relevant knowledge about the potential adverse effects of artificial light at night (ALAN) from research into applicable urban lighting practice. Therefore, the aim of this paper is to identify and report, via a systematic review, the effects of exposure to different physical properties of artificial light sources on various organism groups, including plants, arthropods, insects, spiders, fish, amphibians, reptiles, birds, and non-human mammals (including bats, rodents, and primates). PRISMA 2020 guidelines were used to identify a total of 1417 studies from Web of Science and PubMed. In 216 studies, diverse behavioral and physiological responses were observed across taxa when organisms were exposed to ALAN. The studies showed that the responses were dependent on high illuminance levels, duration of light exposure, and unnatural color spectra at night and also highlighted where research gaps remain in the domains of ALAN research and urban lighting practice.To avoid misinterpretation, and to define a common language, key terminologies and definitions connected to natural and artificial light have been provided. Furthermore, the adverse impacts of ALAN urgently need to be better researched, understood, and managed for the development of future lighting guidelines and standards to optimize sustainable design applications that preserve night-time environment(s) and their inhabiting flora and fauna.
... We found evidence of a negative association between species richness and urbanization. This result may be related to inhospitable characteristics of the urban environment for amphibians, such as artificial light (Baker and Richardson 2006), noise (Leon et al. 2019;Yi and Sheridan 2019), roads (Carr and Fahrig 2001;Pillsbury and Miller 2008), and possible contaminants (Knutson et al. 1999). Such drivers may influence the anuran life cycle in several ways. ...
... Such drivers may influence the anuran life cycle in several ways. Noise pollution and artificial light can directly affect amphibian calling behavior, potentially leading to changes in survival and reproduction rates (Sun and Narins 2005;Baker and Richardson 2006). Heavy metal contamination, such as mercury, lead and copper, may have a range of harmful effects on larvae, including impaired behavioral responsiveness, reduced growth rates and delayed metamorphosis (Hopkins and Rowe 2010;Ficken and Byrne 2013). ...
Article
Full-text available
The rapid expansion of urban areas in which natural and semi-natural areas are replaced by human infrastructure, is a major threat to biodiversity worldwide. However, little is known about how the structure of biotic communities is affected by urbanization in the tropics. Here, we tested the effect of land use types and pond size in urban and rural areas on frog species richness and community composition in central Brazil. We selected 20 ponds differing in size and surrounding levels of urbanization and native vegetation cover. We quantified relationships between environmental variables and species richness and community composition using a Poisson GLM and a distance-based Redundancy Analysis (db-RDA), respectively. Variation in species richness was positively related to pond size and negatively related to the amount of urbanization in a 500 m buffer around ponds. Community composition was mainly driven by species turnover than by nestedness, with turnover being explained primarily by urbanization and native vegetation cover. Our results indicate that urbanization negatively influences species richness. Moreover, as the amount of urbanization increased, several species were replaced by other taxa better adapted to urban environments. Our results indicate that understanding the effects of urbanization on amphibians in tropical cities might improve conservation strategies, such as preserving large ponds in urban environments.
... lx ALAN, adult grey treefrogs, Hyla chrysoscelis, reduce foraging (Buchanan, 1993) and adult red-back salamanders, Plethodon cinereus, exposed to ALAN from string lights (lux not reported but likely low light) reduce activity and foraging (Wise and Buchanan, 2006). Similarly, adult common green frogs, Rana clamitans, reduce advertisement calling when exposed to 52 lxe120 lx ALAN (Baker and Richardson, 2006). Constant light (lux not reported) affects the physiology of tiger salamanders, Ambystoma tigrinum, by disrupting normal oscillating melatonin rhythms associated with normal light/dark cycles (Gern et al., 1983). ...
... Anuran larvae are likely stressed by ALAN as many species are nocturnal and have dark adapted eyes (Baker and Richardson, 2006), circadian rhythms are tied to natural light/dark cycles (Azzi et al., 2014;Botha et al., 2017;Ciarleglio et al., 2011) and changes to circadian rhythms can affect physiological processes (Fonken and Nelson, 2014). ALAN disrupts natural light/dark cycles (Falchi et al., 2016), and disrupts circadian rhythms (Bedrosian et al., 2013;Botha et al., 2017;Dominoni et al., 2013), which can alter glucocorticoid (GC) levels (Ouyang et al., 2015). ...
Article
Artificial light at night (ALAN) alters the natural light dark patterns in ecosystems. ALAN can have a suite of effects on community structure and is a driver of evolutionary processes that influences a range of behavioral and physiological traits. Our understanding of possible effects of ALAN across species amphibians is lacking and research is warranted as ALAN could contribute to stress and declines of amphibian populations, particularly in urban areas. We tested the hypothesis that exposure to constant light or pulsed ALAN would physiologically stress Rio Grande leopard frog (Rana berlandieri) and Gulf Coast toad (Bufo valliceps) tadpoles. We reared tadpoles under constant or pulsed (on and off again) ALAN for 14 days and measured corticosterone release rates over time using a non-invasive water-borne hormone protocol. ALAN treatments did not affect behavior or growth. Tadpoles of both species had higher corticosterone (cort) release rates after 14 days of constant light exposure. Leopard frog tadpoles had lower cort release rates after exposure to pulsed ALAN while toad tadpoles had higher cort release rates. These results suggest that short-term exposure to constant or pulsed light at night may contribute to stress in tadpoles but that each species differentially modulated their cort response to ALAN exposure and a subsequent stressor. This flexibility in the upregulation and downregulation of hypothalamic-pituitary-interrenal axis response may indicate an alternative mechanism for diminishing the deleterious effects of chronic stress. Nonetheless, ALAN should be considered in management and conservation plans for amphibians.
... The spatial spread and intensity of nighttime illumination is predicted to steadily increase (Kyba et al., 2017) especially through the development and widespread adoption of new energy-efficient lighting systems such as the light-emitting diode (LED; Kyba et al., 2017;Donatello et al., 2019). Several studies show that ALAN influences several aspects of an animals' behavior such as timing of activity (de Jong et al., 2017;Eccard et al., 2018), movement Laforge et al., 2019), reproduction (Baker and Richardson, 2006;Russ et al., 2017) and foraging (Bird et al., 2004), which in turn can alter social interactions and group dynamics (Kurvers and Hölker, 2015). Under natural conditions, many animals experience dark nights as periods where the perceived predation risk is low and foraging can be extended or expanded to open habitats. ...
Article
Full-text available
Differences in natural light conditions caused by changes in moonlight are known to affect perceived predation risk in many nocturnal prey species. As artificial light at night (ALAN) is steadily increasing in space and intensity, it has the potential to change movement and foraging behavior of many species as it might increase perceived predation risk and mask natural light cycles. We investigated if partial nighttime illumination leads to changes in foraging behavior during the night and the subsequent day in a small mammal and whether these changes are related to animal personalities. We subjected bank voles to partial nighttime illumination in a foraging landscape under laboratory conditions and in large grassland enclosures under near natural conditions. We measured giving-up density of food in illuminated and dark artificial seed patches and video recorded the movement of animals. While animals reduced number of visits to illuminated seed patches at night, they increased visits to these patches at the following day compared to dark seed patches. Overall, bold individuals had lower giving-up densities than shy individuals but this difference increased at day in formerly illuminated seed patches. Small mammals thus showed carry-over effects on daytime foraging behavior due to ALAN, i.e., nocturnal illumination has the potential to affect intra- and interspecific interactions during both night and day with possible changes in personality structure within populations and altered predator-prey dynamics.
... Since half of all humans, responsible for the light pollution, live within 3 km of surface water bodies, ALAN should also affect freshwater organisms. However, only few studies have investigated the effect of ALAN in freshwater: Frogs are attracted by light sources at night and show a higher activity when ALAN is switched on (Baker and Richardson, 2006). The crustacean genus Gammarus shows a reduced activity in the presence of ALAN (Perkin et al., 2014). ...
Article
Full-text available
Cryptochromes are evolutionary ancient blue-light photoreceptors that are part of the circadian clock in the nervous system of many organisms. Cryptochromes transfer information of the predominant light regime to the clock which results in the fast adjustment to photoperiod. Therefore, the clock is sensitive to light changes and can be affected by anthropogenic Artificial Light At Night (ALAN). This in turn has consequences for clock associated behavioral processes, e.g., diel vertical migration (DVM) of zooplankton. In freshwater ecosystems, the zooplankton genus Daphnia performs DVM in order to escape optically hunting predators and to avoid UV light. Concomitantly, Daphnia experience circadian changes in food-supply during DVM. Daphnia play the keystone role in the carbon-transfer to the next trophic level. Therefore, the whole ecosystem is affected during the occurrence of cyanobacteria blooms as cyanobacteria reduce food quality due to their production of digestive inhibitors (e.g., protease inhibitors). In other organisms, digestion is linked to the circadian clock. If this is also the case for Daphnia, the expression of protease genes should show a rhythmic expression following circadian expression of clock genes (e.g., cryptochrome 2). We tested this hypothesis and demonstrated that gene expression of the clock and of proteases was affected by ALAN. Contrary to our expectations, the activity of one type of proteases (chymotrypsins) was increased by ALAN. This indicates that higher protease activity might improve the diet utilization. Therefore, we treated D. magna with a chymotrypsin-inhibitor producing cyanobacterium and found that ALAN actually led to an increase in Daphnia’s growth rate in comparison to growth on the same cyanobacterium in control light conditions. We conclude that this increased tolerance to protease inhibitors putatively enables Daphnia populations to better control cyanobacterial blooms that produce chymotrypsin inhibitors in the Anthropocene, which is defined by light pollution and by an increase of cyanobacterial blooms due to eutrophication.
... The spatial spread and intensity of nighttime illumination is predicted to steadily increase (Kyba et al., 2017) especially through the development and widespread adoption of new energy-efficient lighting systems such as the light-emitting diode (LED; Kyba et al., 2017;Donatello et al., 2019). Several studies show that ALAN influences several aspects of an animals' behavior such as timing of activity (de Jong et al., 2017;Eccard et al., 2018), movement Laforge et al., 2019), reproduction (Baker and Richardson, 2006;Russ et al., 2017) and foraging (Bird et al., 2004), which in turn can alter social interactions and group dynamics (Kurvers and Hölker, 2015). Under natural conditions, many animals experience dark nights as periods where the perceived predation risk is low and foraging can be extended or expanded to open habitats. ...
Article
Full-text available
Differences in natural light conditions caused by changes in moonlight are known to affect perceived predation risk in many nocturnal prey species. As artificial light at night (ALAN) is steadily increasing in space and intensity, it has the potential to change movement and foraging behavior of many species as it might increase perceived predation risk and mask natural light cycles. We investigated if partial nighttime illumination leads to changes in foraging behavior during the night and the subsequent day in a small mammal and whether these changes are related to animal personalities. We subjected bank voles to partial nighttime illumination in a foraging landscape under laboratory conditions and in large grassland enclosures under near natural conditions. We measured giving-up density of food in illuminated and dark artificial seed patches and video recorded the movement of animals. While animals reduced number of visits to illuminated seed patches at night, they increased visits to these patches at the following day compared to dark seed patches. Overall, bold individuals had lower giving-up densities than shy individuals but this difference increased at day in formerly illuminated seed patches. Small mammals thus showed carry-over effects on daytime foraging behavior due to ALAN, i.e., nocturnal illumination has the potential to affect intra- and interspecific interactions during both night and day with possible changes in personality structure within populations and altered predator-prey dynamics.
... Species living in arid climates often emerge rapidly in response to rainfall including the South American Andean toad Melanophryniscus rubriventris (Vaira 2005) and the spadefoot toad Scaphiopus holbrooki (Greenberg and Tanner 2004). Other cues which have been reported to trigger emergence and attendance at breeding sites are changes in barometric pressures (FitzGerald and Bider 1974;Greenberg and Tanner 2004), photoperiod (Narayan et al. 2010), light intensity (Baker and Richardson 2006;Heinzmann 1970), humidity (Bellis 1962;Walther et al. 2002) and wind (Henzi et al. 1995). ...
Article
Full-text available
In species with explosive breeding strategies, large numbers of individuals may congregate at a defined location for a very short period of time. Effective synchronisation in arrival at breeding sites is crucial to ensure mating success. Amphibians with explosive breeding strategies often congregate at ponds for only a few days or weeks a year. Previous research has shown that frogs and toads may use a variety of exogenous cues to initiate breeding migrations which include temperature, rainfall and lunar cues. Although the effects of temperature and rainfall on amphibians are widely studied and understood, the impacts of lunar phase are poorly known and vary by species and location. In this study, we examined the effects of lunar phase on the numbers of common toads (Bufo bufo) and common frogs (Rana temporaria) migrating to breeding ponds at 43 sites across the UK over 4 years. Our findings show that peak migration of both common toads and common frogs coincides with the waxing phase of the moon, peaking around the full moon. Temperature and rainfall also had an effect on peak migrations with the highest numbers of common toads and common frogs occurring on warm and damp evenings close to a full moon. Our results have implications for amphibian conservation initiatives such as ‘Toads on Roads’ as they will help inform conservationists on the most effective timing to help toads and frogs across roads.
Article
Artificial light at night (ALAN) has rapidly and drastically changed the global nocturnal environment. Evidence for the effect of ALAN on animal behaviour is mounting and animals are exposed to both point sources of light (street and other surrounding light sources) and broadscale illuminance in the form of skyglow. Research has typically taken a simplified approach to assessing the presence of ALAN, yet to fully understand the ecological impact requires consideration of the different scales and sources of light concurrently. Bird song has previously been well studied for its relationship with light, offering an opportunity to examine the relative impact of different sources of light on behaviour. In this study, we combine correlational and experimental approaches to examine how light at night affects the nocturnal song behaviour of the largely diurnal willie wagtail (Rhipidura leucophrys). Observations of willie wagtails across urban and rural locations in southeastern Australia demonstrated that nocturnal song behaviour increased with the intensity of moonlight in darker rural areas but decreased in areas with high sky glow. In addition, willie wagtails were half as likely to sing at night in the presence of localized light sources such as streetlights in urban and rural areas. Experimental introduction of streetlights to a previously dark area confirmed this relationship: willie wagtail song rates declined when lights were turned on and returned to their original rates following streetlight removal. Our findings show that scale, as well as intensity, are important when considering the impact of light at night as moonlight, sky glow, and localized sources of artificial light have different effects on nocturnal song behaviour.
Article
Ambient levels of nonionizing electromagnetic fields (EMF) have risen sharply in the last five decades to become a ubiquitous, continuous, biologically active environmental pollutant, even in rural and remote areas. Many species of flora and fauna, because of unique physiologies and habitats, are sensitive to exogenous EMF in ways that surpass human reactivity. This can lead to complex endogenous reactions that are highly variable, largely unseen, and a possible contributing factor in species extinctions, sometimes localized. Non-human magnetoreception mechanisms are explored. Numerous studies across all frequencies and taxa indicate that current low-level anthropogenic EMF can have myriad adverse and synergistic effects, including on orientation and migration, food finding, reproduction, mating, nest and den building, territorial maintenance and defense, and on vitality, longevity and survivorship itself. Effects have been observed in mammals such as bats, cervids, cetaceans, and pinnipeds among others, and on birds, insects, amphibians, reptiles, microbes and many species of flora. Cyto- and geno-toxic effects have long been observed in laboratory research on animal models that can be extrapolated to wildlife. Unusual multi-system mechanisms can come into play with non-human species — including in aquatic environments — that rely on the Earth’s natural geomagnetic fields for critical life-sustaining information. Part 2 of this 3-part series includes four online supplement tables of effects seen in animals from both ELF and RFR at vanishingly low intensities. Taken as a whole, this indicates enough information to raise concerns about ambient exposures to nonionizing radiation at ecosystem levels. Wildlife loss is often unseen and undocumented until tipping points are reached. It is time to recognize ambient EMF as a novel form of pollution and develop rules at regulatory agencies that designate air as ‘habitat’ so EMF can be regulated like other pollutants. Long-term chronic low-level EMF exposure standards, which do not now exist, should be set accordingly for wildlife, and environmental laws should be strictly enforced — a subject explored in Part 3.
Article
Full-text available
Social interactions are ubiquitous across the animal kingdom. A variety of ecological and evolutionary processes are dependent on social interactions, such as movement, disease spread, information transmission, and density-dependent reproduction and survival. Social interactions, like any behaviour, are context dependent, varying with environmental conditions. Currently, environments are changing rapidly across multiple dimensions, becoming warmer and more variable, while habitats are increasingly fragmented and contaminated with pollutants. Social interactions are expected to change in response to these stressors and to continue to change into the future. However, a comprehensive understanding of the form and magnitude of the effects of these environmental changes on social interactions is currently lacking. Focusing on four major forms of rapid environmental change currently occurring, we review how these changing environmental gradients are expected to have immediate effects on social interactions such as communication, agonistic behaviours, and group formation, which will thereby induce changes in social organisation including mating systems, dominance hierarchies, and collective behaviour. Our review covers intraspecific variation in social interactions across environments, including studies in both the wild and in laboratory settings, and across a range of taxa. The expected responses of social behaviour to environmental change are diverse, but we identify several general themes. First, very dry, variable, fragmented, or polluted environments are likely to destabilise existing social systems. This occurs as these conditions limit the energy available for complex social interactions and affect dissimilar phenotypes differently. Second, a given environmental change can lead to opposite responses in social behaviour, and the direction of the response often hinges on the natural history of the organism in question. Third, our review highlights the fact that changes in environmental factors are not occurring in isolation: multiple factors are changing simultaneously, which may have antagonistic or synergistic effects, and more work should be done to understand these combined effects. We close by identifying methodological and analytical techniques that might help to study the response of social interactions to changing environments, highlight consistent patterns among taxa, and predict subsequent evolutionary change. We expect that the changes in social interactions that we document here will have consequences for individuals, groups, and for the ecology and evolution of populations, and therefore warrant a central place in the study of animal populations, particularly in an era of rapid environmental change.
Article
Astronomers consider light pollution to be a growing problem, however few studies have addressed potential effects of light pollution on wildlife. Sunlight is believed to initiate song in many bird species. If light initiates song, then light pollution may be influencing avian song behavior at a population level. This hypothesis predicts that birds breeding in areas with large amounts of artificial light will begin singing earlier in the day than birds in areas with little artificial light. Birds in highly illuminated areas might begin singing earlier than did birds in those same areas in previous years when artificial light levels were known to be, or were presumably, lower. Also, birds should begin singing earlier within a site on brightly lit nights. In 2002 and 2003 I documented initiation of morning song by breeding American Robins (Turdus migratorius) in areas with differing intensity of artificial nocturnal light. I compared my observations among sites and against historical studies. Robin populations in areas with large amounts of artificial light frequently began their morning chorus during true night. Chorus initiation time, relative to civil twilight, was positively correlated with amount of artificial light present during true night. Robin choruses in areas with little, or presumably little, artificial light have almost never begun during true night, instead appearing to track the onset of civil twilight. Proliferation of artificial nocturnal light may be strongly affecting singing behavior of American Robins at a population level.
Article
Field studies were conducted on factor affecting embryo mortality in bullfrogs, Rana catesbeiana, in 1975 and 1976 at the E. S. George Reserve of the University of Michigan. Larger @V produced significantly larger clutches than smaller @V (6000 to >20,000). Older @V produced 2 clutches each year with 2nd clutches containing significantly fewer eggs than 1st clutches. Egg size appeared to be unrelated to @V size; however, 2nd clutches contained significantly smaller eggs than initial clutches for all @V @V. Embryo mortality depended on @V choice of oviposition sites. Such sites were controlled by territorial @M @M. Larger @M @M controlled oviposition sites that had significantly lower embryo mortality than the sites of smaller @M @M. Sources of embryo mortality included developmental abnormalities and predation. Choice of oviposition sites included: (a) advance of areas with high water temperatures (>32 degrees C) that result in increased developmental abnormalities and (b) preference for areas that increase embryo survival by increasing developmental rate and/or decreasing efficiency of predation on embryos by the leech. Macrobdella decora.
Article
Vertebrate rod photoreceptors adjust their sensitivity as they adapt during exposure to steady light. Light adaptation prevents the rod from saturating and significantly extends its dynamic range. We examined the time course of the onset of light adaptation in bullfrog rods and compared it with the projected onset of feedback reactions thought to underlie light adaptation on the molecular level. We found that adaptation developed in two distinct temporal phases: (1) a fast phase that operated within seconds after the onset of illumination, which is consistent with most previous reports of a 1–2-s time constant for the onset of adaptation; and (2) a slow phase that engaged over tens of seconds of continuous illumination. The fast phase desensitized the rods as much as 80-fold, and was observed at every light intensity tested. The slow phase was observed only at light intensities that suppressed more than half of the dark current. It provided an additional sensitivity loss of up to 40-fold before the rod saturated. Thus, rods achieved a total degree of adaptation of ∼3,000-fold. Although the fast adaptation is likely to originate from the well characterized Ca2+-dependent feedback mechanisms regulating the activities of several phototransduction cascade components, the molecular mechanism underlying slow adaptation is unclear. We tested the hypothesis that the slow adaptation phase is mediated by cGMP dissociation from noncatalytic binding sites on the cGMP phosphodiesterase, which has been shown to reduce the lifetime of activated phosphodiesterase in vitro. Although cGMP dissociated from the noncatalytic binding sites in intact rods with kinetics approximating that for the slow adaptation phase, this hypothesis was ruled out because the intensity of light required for cGMP dissociation far exceeded that required to evoke the slow phase. Other possible mechanisms are discussed.
Article
Foraging behavior is responsive to changes in predation risk; increased illumination reduces foraging in open areas without cover. Foraging behavior is also affected by resource enrichments. Differences among species in habitat selection are correlated with specific abilities to detect and avoid predators. The least vulnerable species, Dipodomys deserti, foraged heavily in the open and was largely unaffected by treatments; the other species of kangaroo rats and kangaroo mice (D. merriami, D. microps, and Microdipodops pallidus) also prefer the open, but responded to both risk and resource manipulations; highly vulnerable Peromyscus maniculatus was restricted to bushes, even under the best of circumstances; Perognathus longimembris was displaced from preferred microhabitats by the presence of kangaroo rats. Predation risk provides an axis along which habitat segregation occurs. -from Author