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Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia
Journal Pre-proofs Short communication Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia Samantha Wanjiru Mbugua, Choong Hay Wong, Shyamala Ratnayeke PII: DOI: Reference:
S1226-8615(19)30560-6 https://doi.org/10.1016/j.aspen.2019.10.005 ASPEN 1453
To appear in:
Journal of Asia-Pacific Entomology
Received Date: Revised Date: Accepted Date:
27 August 2019 11 October 2019 17 October 2019
Please cite this article as: S. Wanjiru Mbugua, C. Hay Wong, S. Ratnayeke, Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia, Journal of Asia-Pacific Entomology (2019), doi: https://doi.org/10.1016/j.aspen.2019.10.005
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
1
Abstract
2
Firefly populations are threatened globally by habitat alteration, pesticide use, and anthropogenic
3
sources of light. Lamprigera fireflies were recently reported at an urban city park in Kuala
4
Lumpur, Peninsular Malaysia. Here we report on the responses of Lamprigera larvae to artificial
5
light from street lamps on paved park trails. Larvae were located farther from artificial light
6
sources when street lamps were illuminated than when they were not, and mostly where light
7
intensities were lowest, off park trails. Larvae that were located within the direct field of
8
illumination tended to be immobile, whereas, when street lamps were turned off, they actively
9
travelled paved trails. Larvae positioned directly in the path of downwelling light from street
10
lamps at dusk may therefore experience an effectively longer diurnal period, limited time for
11
active foraging, and greater exposure to pedestrian traffic.
12
Keywords: Artificial light, street lamps, mobility, light intensity, light disturbance.
13 14
Introduction
15
Fireflies are bioluminescent beetles in the Lampyridae family, Order Coleoptera, found in
16
temperate and tropical zones all over the world. The larvae prey on a variety of small
17
invertebrates and represent the principle feeding stage of the lampyrid life cycle. Firefly larvae
18
are therefore ecologically and economically important for their potential to regulate populations
19
of invertebrate prey in natural and agricultural ecosystems (Rios & Quinta 2010, Wijekoon et al.
20
2016).
21
Insect diversity and abundance is dwindling rapidly (Hallmann et. al. 2017). Firefly populations
22
across many global regions are threatened by habitat alteration (Sánchez-Bayo & Wyckhuys,
23
2019), the widespread use of pesticides (Tabaru et al. 1970, Disque et al. 2018) and light
24
pollution (Hölker et al. 2010, Firebaugh & Haynes 2016). The latter may be particularly harmful
25
to nocturnal fireflies, which are adapted to lowlight habitats and rely on bioluminescence to
26
recognize potential mates (Owens et al. 2008). Of more than 2000 estimated species of firefly,
27
the genus Lamprigera, possesses the largest larvae of all fireflies in Eurasia (Fig. 1). Formerly
28
classified under the subfamily Lampyrinae, a recent phylogenetic study based on mitochondrial
29
COI sequences indicates that Lamprigera forms a separate clade, basal to all extant firefly
30
groups and is thus an ancient and unique taxon of the Lampyridae (Liu et al. 2017).
31
Females of Lamprophorus (Lamprigera) tenebrosus are apterous, ~7 cm, with a larviform
32
appearance (Fig. 1), possessing a pale creamy colour (Brues 1941). According to Hutson and
33
Austin (1924) adult males and females live about 2 weeks and 2-3 months, respectively; adult
34
males (~2.5 cm) are winged and attracted to light emitted by females who on average lay up to
35
66 eggs in the soil and die shortly after eggs hatch. Larvae may reach lengths of 7 cm and live 8-
36
9 months in captivity. Pupation occurs under the soil and takes 7-10 days for females and 16-23
37
days for males (Hutson & Austin 1924). Larvae in this genus are nocturnal and shelter in damp
38
leaf litter, or within soil, 6 – 8 inches from the soil surface during the day (Bess 1956).
39
Lamprigera larvae are voracious feeders of snails and can be seen actively crawling around in
40
search of prey at night (Bess 1956, Wijekoon et al. 2016).
41
Recent reports confirmed for the first time, the presence of Lamprigera sp. larvae at an urban
42
city park in Kuala Lumpur, Peninsular Malaysia (Chan, 2017). The park provides valuable
43
greenspace for urbanites, receiving abundant visitors during the day and early hours of the night,
44
(Nair 2016). Street lamps illuminate the main paved trail of the park for a few hours each night
45
to permit evening use by joggers and cyclists. Larvae of holometabolous insects possess single-
46
lens light receptors or stemmata that are sensitive to motion, colour and polarization (Meyer-
47
Rochow 1974). The anatomy of stemmata in Photuris firefly larvae suggest that their eyes are
48
optimized for capturing the maximum light possible and thus adapted for nocturnal activity.
49
Stemmata in insect larvae may play an important role in photoperiodism (Shintani et al. 2009),
50
predator avoidance, prey detection, and navigation (Murphy & Moiseff, 2018). For example,
51
counts of larvae of the nocturnal glow worm Lampyris noctiluca decline sharply during the full
52
moon (Gunn and Gunn 2012) and onset of larval activity is strongly influenced by low ambient
53
light conditions (Driesig 1974). Artificial light at night (ALAN) is temporally disorienting to
54
adult activity cycles but little is known about its effects on larvae (Owens and Lewis 2018).
55
Lamprigera larvae are nocturnally active and possess stemmata (Fig. 1); they are therefore
56
capable of sensing and responding to photic stimulation and thus vulnerable to the effects of
57
ALAN. This communication reports on the responses of Lamprigera larvae to artificial light
58
sources at night, which is when larvae actively move about in search of prey. We hypothesized
59
that larvae would maintain greater distances on average from street lamps when they were turned
60
on and that light intensity influenced this relationship.
61 62
Materials and Methods
63
We studied larvae responses to artificial light from April - May 2019 at Taman Persekutuan
64
Bukit Kiara (3º 8’ 31’’N, 101º 38’ 32’’ E), a 190 ha secondary forest enclave within the city of
65
Kuala Lumpur, Malaysia. Four paved trails (~ 10 km) lined with street lamps fitted with light
66
emitting diodes (LED) light fixtures intersected the park and received heavy use by hikers,
67
joggers, and cyclists until 22:00 hrs. The curb on either side of trails consisted of a 2-5 m radius
68
of mowed grass beyond which trees and shrubs occurred. Sampling was conducted along 2-km
69
transects between 19:30 (sunset) and 01:00 hrs. Street lamps were lit at 19:00 hrs and switched
70
off at 22:00 hrs. At locations where larvae were observed, we measured the distance of the larva
71
to the base of the nearest street lamp and used a light meter (KK Instruments CEN0063 750) to
72
measure light intensity in lux at the position where the larva was located. This procedure was
73
repeated ~15 minutes on average after lights were off. On nights uninterrupted by rain, 20 or
74
more larvae of various sizes/instars (3 – 6 cm) were detected along a 2-km transect. We used a
75
t-test of unequal variance to compare the mean distances of larvae to the base of the nearest
76
street lamp when lights were on versus off. Light intensity differed with distance and angle from
77
the base of street lamps because lamps were positioned to project the maximum light on paved
78
trails rather than the curb-side. As a consequence, light intensity 3 m from the base of the street
79
lamp could differ depending on whether it was measured on the paved trail or on the curb-side.
80
Thus, we report the frequency of locating larvae at different ranges of artificial light intensity.
81
We used a Pearson correlation test to test whether larval distances from illuminated street lamps
82
declined with time, after street lamps were turned off. We used a Chi2 2 x 2 contingency test to
83
compare associations between larval use of paved trails and vegetated curbs when street lights
84
were “on” versus “off”.
85 86
Results
87
Lamprigera larvae were located farther on average from street lamps when they were on (N=
88
41), than when they were off (N= 123; Fig. 2, df = 66, T = 2.29 , p = 0.025), and larvae were less
89
likely to be located within regions of street lamp intensity (Fig. 3). The difference in sample size
90
owed partly to sampling effort: sampling in the early hours of the night was often curtailed
91
because of heavy rain. A few larvae that were situated very close to illuminated lamp posts under
92
high light intensity exhibited limited movement. However, when street lamps were turned off,
93
Lamprigera larvae were observed actively moving along paved trails and adjacent grass/shrub
94
thickets. Larval distance to street lamps did not alter significantly with time after street lamps
95
were turned off at 22:00 (Fig. 4, N= 156, adjusted r2 = -0.004, p = 0.526), but larvae were
96
observed to actively travel paved trails more than expected when street lamps were off (Fig. 5,
97
Chi2 2 x 2 contingency test, χ2= 8.63, df = 1, p = 0.003).
98 99
Discussion
100
Lamprigera larvae tend to maintain slightly greater distances from illuminated street lamps at
101
night and were less likely to be found in areas with high artificial light intensity. Street lamps
102
were positioned to project the maximum light on paved trails. We speculate that when street
103
lights were turned on, larvae along dimly lit parts of the trail were capable of mobilizing and
104
avoiding regions of intense artificial light, but those directly exposed to the glare of the street
105
lamps, were often stationary. Because Lamprigera larvae are quite mobile, once street lamps
106
were turned off, movements relative to lamp positions seemed more random, with more larvae
107
travelling the unlit paved trails.
108
A possible caveat to our data is that larvae were easier to locate when lights were off. However,
109
Lamprigera larvae are large and conspicuous, emit a continuous glow, which is easily detectable
110
except under bright light, and there were four observers to locate larvae. Thus, it is unlikely that
111
active larvae went undetected when lights were on. We propose that, larvae within range of high
112
light intensities emitted by street lamps remained hidden, and thus undetected, in crevices and
113
under leaf litter, becoming active and detectable only after lamps were switched off. Bess (1956)
114
confirms that Lamprophorus (Lamprigera) tenebrosus larvae in Sri Lanka hide in soil and leaf
115
litter during the day.
116
Lamprigera larvae were never seen during daylight at this site suggesting that they are negatively
117
phototactic to light and may not move around until dark. Because street lamps are turned off,
118
well before sunrise, larvae that bed down close to a street lamp, may end up directly within the
119
radius of high intensity light when street lamps are turned on. These individuals may not detect a
120
change in photoperiod at dusk because street lamps are turned on before sunset. Artificial light
121
may therefore impose costs to these larvae by limiting the time they engage in foraging. In this
122
specific urban situation, failing to move away from illuminated street lamps may also expose
123
larvae to greater risks from cyclist and pedestrian traffic.
124
Firefly larvae and other nocturnal ground insects are likely to be affected by downwelling light
125
such as street lamps (Owens 2008, Owens & Lewis 2018). Future work on the behavioral
126
responses of individual Lamprigera larvae to different intensities of artificial light including
127
other forms of human activity will help to confirm thresholds of disturbance. Nevertheless,
128
Lamprigera larvae seem abundant at this specific urban location of Peninsular Malaysia,
129
although ground maintenance such as mowing grass and clearing leaf litter along trails seem to
130
cause marked declines in larval counts. Leaf litter may provide important shelter for larvae.
131
Although two adult females were observed during the study, adult males have never been
132
captured at this location. To our knowledge, this study contributes to the first quantitative
133
corroboration of artificial light effects on larval fireflies.
134 135
Acknowledgments
136
We are grateful to Teo Boon Ping for logistical support and to Lee Sang Soon and Lee Jia Jie for
137
assistance with data collection. We thank the administrators of Bukit Kiara, especially Mr. Melvin
138
Santhanumsamy, for permission to work on the site at night. Funding was provided by the
139
Department of Biological Sciences, Sunway University.
140 141
References
142
Bess, H.A., 1956., Ecological notes on Lamprophorus tenebrosus (Walker) (Coleoptera:
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Lampyridae), an enemy of the Giant African Snail, Proceedings, Hawaiian Entomological
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Society xvi(1), 24-29.
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Brues, C.T. 1941., Characteristics of the Larviform Female of the Lampyrid Beetle,
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Lamprophorus. Psyche 48, 41-44. Available at: https://doi.org/10.1155/1941/60591 [Date
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Chan, E. 2017., The world’s largest firefly can be found in Kuala Lumpur. Available at
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https://www.star2.com/living/living-environment/2017/08/12/world-largest-
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firefly/#s1HQCJOqcWHGdv7v.99. [Date accessed: 4 Jul, 2019]
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Dreisig, H., 1974. Observations on the luminescence of the larval glowworm, Lampyris noctiluca. Entomologica scandinavica 5, 103–109.
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Disque, H.H., Hamby, K.A., Dube, A., Taylor, C., Dively, G.P., 2018. Effects of clothianidin-
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treated seed on the arthropod community in a mid-Atlantic no-till corn agroecosystem.
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Firebaugh, A., Haynes, K. 2016., Experimental tests of light-pollution impact on nocturnal
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insect courtship and dispersal. Oecologia, 182(4), 1203-1211. doi:10.1007/s00442-
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016-3723-1.
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Hallmann, C.A., Sorg, M., Jongejans, E., Siepel, H., Hofland, N., Schwan, H. et al., 2017. More
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than 75 percent decline over 27 years in total flying insect biomass in protected
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areas. PLoS One, 12, e0185809, https://doi.org/10.1371/journal.pone.0185809. [Date
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accessed: 4 Jul 2019]
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Hölker, F., Wolter, C., Perkin, E.K., Tockner, K., 2010. Light pollution as a biodiversity threat. Trends in Ecology & Evolution, 25, 681– 682. Hsiao, H.S., 1973. Flight paths of night-flying moths to light. Journal of Insect Physiology, 19(10), 1971–1976. doi:10.1016/0022-1910(73)90191-1. Hutson, J.C., G.D. Austin., 1924. Notes on the habits and life-history of the Indian glow-worm.
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An enemy of the African or Kalutara snail. Ceylon Department of Agriculture Bulletin
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69, 1–15.
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Liu G.C., Dong, Z.W., He, J.W., Zhao, R.P., Wang, W., Li, X.Y., 2017. Genome size of 14 species of fireflies (Insecta, Coleoptera, Lampyridae). Zoological Research 38, 449-458. Meyer-Rochow, V. B. 1974 Structure and function of the larval eye of the sawfly, Perga. Journal of Insect Physiology, 20, 1565-1591. Murphy, F., Moiseff, A. 2019.Anatomy of the stemmata in the Photuris firefly larva. Journal of Comparative Physiology A, 205:151-161. Doi:10.1007/s00359-018-01312-2.
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Nair, V. 2016., Walk to save Bukit Kiara. Available at:
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https://www.thestar.com.my/metro/community/2016/01/27/fighting-for-bukit-kiara.
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[Date accessed: 6 October 2019]
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Owens, A.C.S., Meyer-Rochow, V.B., Yang, E.C., 2008. Short- and mid-wavelength artificial
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light influences the flash signals of Aquatica ficta fireflies (Coleoptera: Lampyridae).
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PLoS ONE 13(2): e0191576. Available at: https://doi.org/10.1371/journal.pone.0191576.
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[Date accessed: 1 October 2019]
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Owens, A.C.S, Lewis, S.M., 2018. The impact of artificial light at night on nocturnal insects: A review and synthesis. Ecology and Evolution,8(22), 11337-11358. Rios, O.M., Quinta, M.H., 2010. Larval Feeding Habits of the Cuban Endemic Firefly
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Alecton discoidalis Laporte (Coleoptera: Lampyridae). Psyche 2010, Article ID 149879,
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Available at: http://dx.doi.org/10.1155/2010/149879 [Date accessed: 10 May, 2019]
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Sánchez-Bayo, F., Wyckhuys, K.A., 2019. Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation 232, 8–27. Shintani, Y., Shiga, S., Numata, H., 2009. Different photoreceptor organs are used for
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photoperiodism in the larval and adult stages of the carabid beetle, Leptocarabus
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kumagaii. Journal of Experimental Biology 212, 3651-3655; doi: 10.1242/jeb.034033
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Tabaru, Y., Kouketsu, T., Oba, M., Okafuji, S., 1970. Effects of some organophosphorus
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insecticides against the larvae of Genji firefly, Luciola cruciata Motschulsky
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(Lampyridae:Coleoptera) and their prey, Japanese melanial snail, Semisulcospira
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bensoni Phillipi (Pleuroceridae: Mesogastropoda). Medical Entomology and Zoology
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21, 178–181
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Wijekoon, W.M.C.D., Wegiriya, H.C.E., Bogahawatta, C.N.L., 2016. Predatory role of
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Lampyrid larvae (Lamprigera tenebrosa); laboratory experiments to control
202
agricultural molluscan pests, Achatina fullica & Laevicualis altae. International
203
Journal of Science, Environment and Technology, 5, 1-6.
204
205
Figure Legends
206
Fig. 1. Dorsal (A) and dorso-lateral (B) views of the larva and adult female (C; not to scale) of
207
the Lamprigera firefly at Taman Persekutuan Bukit Kiara (Federal Park), Kuala Lumpur,
208
Malaysia. Red arrows in B denote position of larval eyes. Adult females of this genus are
209
apterous or flightless. Lee Sang Soon contributed photographs A and B.
210
Fig. 2. A comparison of the mean distances of Lamprigera spp. larvae to the nearest street lamps
211
when they were switched on (1900 – 2200 hrs, N = 41) and switched off (2201 hrs – 0100 hrs, N
212
= 123).
213
Fig. 3. Frequencies at which Lamprigera larvae were located at different ranges of light intensity
214
when street lamps were illuminated at night. Larvae were less likely to use areas where light
215
intensity exceeded 3 lux.
216
Fig. 4. Changes in larval distance to the base of street lamps with time after street lamps were
217
turned off at 22:00 hrs. Distances of larvae to street lamps declined slightly with time, but the
218
difference was not significant.
219
Fig. 5. Percentages of larvae located on and off paved trails when street lights were on versus
220
off. Street lamps were positioned to radiate the maximum light on paved trails for human
221
pedestrians. Larvae were more likely to be seen off paved trails overall, but used paved trails less
222
than expected when street lamps were on.
223 224 225
Title: Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia.
226
Authors: Samantha Wanjiru Mbuguaa, Choong Hay Wongb, Shyamala Ratnayekea*
227 228
aDepartment
229 230
bMalaysian
of Biological Sciences, Sunway University, Bandar Sunway, Selangor DE 47500,
Malaysia Nature Society, JKR641, Jalan Kelantan Bukit Persekutuan, 50480 Kuala Lumpur,
Malaysia
231 232
*Corresponding
authors
233 234
Email addresses: [email protected] (S. W. Mbugua), [email protected] (C. H. Wong), [email protected] (S. Ratnayeke)
235 236
Abstract
237
246
Firefly populations are threatened globally by habitat alteration, pesticide use, and anthropogenic sources of light. Lamprigera fireflies were recently reported at an urban city park in Kuala Lumpur, Peninsular Malaysia. Here we report on the responses of Lamprigera larvae to artificial light from street lamps on paved park trails. Larvae were located farther from artificial light sources when street lamps were illuminated than when they were not, and mostly where light intensities were lowest, off park trails. Larvae that were located within the direct field of illumination tended to be immobile, whereas, when street lamps were turned off, they actively travelled paved trails. Larvae positioned directly in the path of downwelling light from street lamps at dusk may therefore experience an effectively longer diurnal period, limited time for active foraging, and greater exposure to pedestrian traffic.
247
Keywords: Artificial light, street lamps, mobility, light intensity, light disturbance.
238 239 240 241 242 243 244 245
248 249 250
We studied responses of Lamprigera larvae to artificial light from street lamps
251
Larvae were active only at night
252
Larvae were farther from street lamps when they were on
253
Larvae within areas of intense artificial light were usually immobile
254 255
256
Figure Captions
257
Fig. 1. Dorsal (A) and dorso-lateral (B) views of the larva and adult female (C; not to scale) of
258
the Lamprigera firefly at Taman Persekutuan Bukit Kiara (Federal Park), Kuala Lumpur,
259
Malaysia. Red arrows in B denote position of larval eyes. Adult females of this genus are
260
apterous or flightless. Lee Sang Soon contributed photographs A and B.
261
Fig. 2. A comparison of the mean distances of Lamprigera spp. larvae to the nearest street lamps
262
when they were switched on (1900 – 2200 hrs, N = 41) and switched off (2201 hrs – 0100 hrs, N
263
= 123).
264
Fig. 3. Frequencies at which Lamprigera larvae were located at different ranges of light intensity
265
when street lamps were illuminated at night. Larvae were less likely to use areas where light
266
intensity exceeded 3 lux.
267
Fig. 4. Changes in larval distance to the base of street lamps with time after street lamps were
268
turned off at 22:00 hrs. Distances of larvae to street lamps declined slightly with time, but the
269
difference was not significant.
270
Fig. 5. Percentages of larvae located on and off paved trails when street lights were on versus
271
off. Street lamps were positioned to radiate the maximum light on paved trails for human
272
pedestrians. Larvae were more likely to be seen off paved trails overall, but used paved trails less
273
than expected when street lamps were on.
274 275
S1226-8615(19)30560-6 https://doi.org/10.1016/j.aspen.2019.10.005 ASPEN 1453
To appear in:
Journal of Asia-Pacific Entomology
Received Date: Revised Date: Accepted Date:
27 August 2019 11 October 2019 17 October 2019
Please cite this article as: S. Wanjiru Mbugua, C. Hay Wong, S. Ratnayeke, Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia, Journal of Asia-Pacific Entomology (2019), doi: https://doi.org/10.1016/j.aspen.2019.10.005
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2019 Korean Society of Applied Entomology. Published by Elsevier B.V. All rights reserved.
1
Abstract
2
Firefly populations are threatened globally by habitat alteration, pesticide use, and anthropogenic
3
sources of light. Lamprigera fireflies were recently reported at an urban city park in Kuala
4
Lumpur, Peninsular Malaysia. Here we report on the responses of Lamprigera larvae to artificial
5
light from street lamps on paved park trails. Larvae were located farther from artificial light
6
sources when street lamps were illuminated than when they were not, and mostly where light
7
intensities were lowest, off park trails. Larvae that were located within the direct field of
8
illumination tended to be immobile, whereas, when street lamps were turned off, they actively
9
travelled paved trails. Larvae positioned directly in the path of downwelling light from street
10
lamps at dusk may therefore experience an effectively longer diurnal period, limited time for
11
active foraging, and greater exposure to pedestrian traffic.
12
Keywords: Artificial light, street lamps, mobility, light intensity, light disturbance.
13 14
Introduction
15
Fireflies are bioluminescent beetles in the Lampyridae family, Order Coleoptera, found in
16
temperate and tropical zones all over the world. The larvae prey on a variety of small
17
invertebrates and represent the principle feeding stage of the lampyrid life cycle. Firefly larvae
18
are therefore ecologically and economically important for their potential to regulate populations
19
of invertebrate prey in natural and agricultural ecosystems (Rios & Quinta 2010, Wijekoon et al.
20
2016).
21
Insect diversity and abundance is dwindling rapidly (Hallmann et. al. 2017). Firefly populations
22
across many global regions are threatened by habitat alteration (Sánchez-Bayo & Wyckhuys,
23
2019), the widespread use of pesticides (Tabaru et al. 1970, Disque et al. 2018) and light
24
pollution (Hölker et al. 2010, Firebaugh & Haynes 2016). The latter may be particularly harmful
25
to nocturnal fireflies, which are adapted to lowlight habitats and rely on bioluminescence to
26
recognize potential mates (Owens et al. 2008). Of more than 2000 estimated species of firefly,
27
the genus Lamprigera, possesses the largest larvae of all fireflies in Eurasia (Fig. 1). Formerly
28
classified under the subfamily Lampyrinae, a recent phylogenetic study based on mitochondrial
29
COI sequences indicates that Lamprigera forms a separate clade, basal to all extant firefly
30
groups and is thus an ancient and unique taxon of the Lampyridae (Liu et al. 2017).
31
Females of Lamprophorus (Lamprigera) tenebrosus are apterous, ~7 cm, with a larviform
32
appearance (Fig. 1), possessing a pale creamy colour (Brues 1941). According to Hutson and
33
Austin (1924) adult males and females live about 2 weeks and 2-3 months, respectively; adult
34
males (~2.5 cm) are winged and attracted to light emitted by females who on average lay up to
35
66 eggs in the soil and die shortly after eggs hatch. Larvae may reach lengths of 7 cm and live 8-
36
9 months in captivity. Pupation occurs under the soil and takes 7-10 days for females and 16-23
37
days for males (Hutson & Austin 1924). Larvae in this genus are nocturnal and shelter in damp
38
leaf litter, or within soil, 6 – 8 inches from the soil surface during the day (Bess 1956).
39
Lamprigera larvae are voracious feeders of snails and can be seen actively crawling around in
40
search of prey at night (Bess 1956, Wijekoon et al. 2016).
41
Recent reports confirmed for the first time, the presence of Lamprigera sp. larvae at an urban
42
city park in Kuala Lumpur, Peninsular Malaysia (Chan, 2017). The park provides valuable
43
greenspace for urbanites, receiving abundant visitors during the day and early hours of the night,
44
(Nair 2016). Street lamps illuminate the main paved trail of the park for a few hours each night
45
to permit evening use by joggers and cyclists. Larvae of holometabolous insects possess single-
46
lens light receptors or stemmata that are sensitive to motion, colour and polarization (Meyer-
47
Rochow 1974). The anatomy of stemmata in Photuris firefly larvae suggest that their eyes are
48
optimized for capturing the maximum light possible and thus adapted for nocturnal activity.
49
Stemmata in insect larvae may play an important role in photoperiodism (Shintani et al. 2009),
50
predator avoidance, prey detection, and navigation (Murphy & Moiseff, 2018). For example,
51
counts of larvae of the nocturnal glow worm Lampyris noctiluca decline sharply during the full
52
moon (Gunn and Gunn 2012) and onset of larval activity is strongly influenced by low ambient
53
light conditions (Driesig 1974). Artificial light at night (ALAN) is temporally disorienting to
54
adult activity cycles but little is known about its effects on larvae (Owens and Lewis 2018).
55
Lamprigera larvae are nocturnally active and possess stemmata (Fig. 1); they are therefore
56
capable of sensing and responding to photic stimulation and thus vulnerable to the effects of
57
ALAN. This communication reports on the responses of Lamprigera larvae to artificial light
58
sources at night, which is when larvae actively move about in search of prey. We hypothesized
59
that larvae would maintain greater distances on average from street lamps when they were turned
60
on and that light intensity influenced this relationship.
61 62
Materials and Methods
63
We studied larvae responses to artificial light from April - May 2019 at Taman Persekutuan
64
Bukit Kiara (3º 8’ 31’’N, 101º 38’ 32’’ E), a 190 ha secondary forest enclave within the city of
65
Kuala Lumpur, Malaysia. Four paved trails (~ 10 km) lined with street lamps fitted with light
66
emitting diodes (LED) light fixtures intersected the park and received heavy use by hikers,
67
joggers, and cyclists until 22:00 hrs. The curb on either side of trails consisted of a 2-5 m radius
68
of mowed grass beyond which trees and shrubs occurred. Sampling was conducted along 2-km
69
transects between 19:30 (sunset) and 01:00 hrs. Street lamps were lit at 19:00 hrs and switched
70
off at 22:00 hrs. At locations where larvae were observed, we measured the distance of the larva
71
to the base of the nearest street lamp and used a light meter (KK Instruments CEN0063 750) to
72
measure light intensity in lux at the position where the larva was located. This procedure was
73
repeated ~15 minutes on average after lights were off. On nights uninterrupted by rain, 20 or
74
more larvae of various sizes/instars (3 – 6 cm) were detected along a 2-km transect. We used a
75
t-test of unequal variance to compare the mean distances of larvae to the base of the nearest
76
street lamp when lights were on versus off. Light intensity differed with distance and angle from
77
the base of street lamps because lamps were positioned to project the maximum light on paved
78
trails rather than the curb-side. As a consequence, light intensity 3 m from the base of the street
79
lamp could differ depending on whether it was measured on the paved trail or on the curb-side.
80
Thus, we report the frequency of locating larvae at different ranges of artificial light intensity.
81
We used a Pearson correlation test to test whether larval distances from illuminated street lamps
82
declined with time, after street lamps were turned off. We used a Chi2 2 x 2 contingency test to
83
compare associations between larval use of paved trails and vegetated curbs when street lights
84
were “on” versus “off”.
85 86
Results
87
Lamprigera larvae were located farther on average from street lamps when they were on (N=
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41), than when they were off (N= 123; Fig. 2, df = 66, T = 2.29 , p = 0.025), and larvae were less
89
likely to be located within regions of street lamp intensity (Fig. 3). The difference in sample size
90
owed partly to sampling effort: sampling in the early hours of the night was often curtailed
91
because of heavy rain. A few larvae that were situated very close to illuminated lamp posts under
92
high light intensity exhibited limited movement. However, when street lamps were turned off,
93
Lamprigera larvae were observed actively moving along paved trails and adjacent grass/shrub
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thickets. Larval distance to street lamps did not alter significantly with time after street lamps
95
were turned off at 22:00 (Fig. 4, N= 156, adjusted r2 = -0.004, p = 0.526), but larvae were
96
observed to actively travel paved trails more than expected when street lamps were off (Fig. 5,
97
Chi2 2 x 2 contingency test, χ2= 8.63, df = 1, p = 0.003).
98 99
Discussion
100
Lamprigera larvae tend to maintain slightly greater distances from illuminated street lamps at
101
night and were less likely to be found in areas with high artificial light intensity. Street lamps
102
were positioned to project the maximum light on paved trails. We speculate that when street
103
lights were turned on, larvae along dimly lit parts of the trail were capable of mobilizing and
104
avoiding regions of intense artificial light, but those directly exposed to the glare of the street
105
lamps, were often stationary. Because Lamprigera larvae are quite mobile, once street lamps
106
were turned off, movements relative to lamp positions seemed more random, with more larvae
107
travelling the unlit paved trails.
108
A possible caveat to our data is that larvae were easier to locate when lights were off. However,
109
Lamprigera larvae are large and conspicuous, emit a continuous glow, which is easily detectable
110
except under bright light, and there were four observers to locate larvae. Thus, it is unlikely that
111
active larvae went undetected when lights were on. We propose that, larvae within range of high
112
light intensities emitted by street lamps remained hidden, and thus undetected, in crevices and
113
under leaf litter, becoming active and detectable only after lamps were switched off. Bess (1956)
114
confirms that Lamprophorus (Lamprigera) tenebrosus larvae in Sri Lanka hide in soil and leaf
115
litter during the day.
116
Lamprigera larvae were never seen during daylight at this site suggesting that they are negatively
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phototactic to light and may not move around until dark. Because street lamps are turned off,
118
well before sunrise, larvae that bed down close to a street lamp, may end up directly within the
119
radius of high intensity light when street lamps are turned on. These individuals may not detect a
120
change in photoperiod at dusk because street lamps are turned on before sunset. Artificial light
121
may therefore impose costs to these larvae by limiting the time they engage in foraging. In this
122
specific urban situation, failing to move away from illuminated street lamps may also expose
123
larvae to greater risks from cyclist and pedestrian traffic.
124
Firefly larvae and other nocturnal ground insects are likely to be affected by downwelling light
125
such as street lamps (Owens 2008, Owens & Lewis 2018). Future work on the behavioral
126
responses of individual Lamprigera larvae to different intensities of artificial light including
127
other forms of human activity will help to confirm thresholds of disturbance. Nevertheless,
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Lamprigera larvae seem abundant at this specific urban location of Peninsular Malaysia,
129
although ground maintenance such as mowing grass and clearing leaf litter along trails seem to
130
cause marked declines in larval counts. Leaf litter may provide important shelter for larvae.
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Although two adult females were observed during the study, adult males have never been
132
captured at this location. To our knowledge, this study contributes to the first quantitative
133
corroboration of artificial light effects on larval fireflies.
134 135
Acknowledgments
136
We are grateful to Teo Boon Ping for logistical support and to Lee Sang Soon and Lee Jia Jie for
137
assistance with data collection. We thank the administrators of Bukit Kiara, especially Mr. Melvin
138
Santhanumsamy, for permission to work on the site at night. Funding was provided by the
139
Department of Biological Sciences, Sunway University.
140 141
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Figure Legends
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Fig. 1. Dorsal (A) and dorso-lateral (B) views of the larva and adult female (C; not to scale) of
207
the Lamprigera firefly at Taman Persekutuan Bukit Kiara (Federal Park), Kuala Lumpur,
208
Malaysia. Red arrows in B denote position of larval eyes. Adult females of this genus are
209
apterous or flightless. Lee Sang Soon contributed photographs A and B.
210
Fig. 2. A comparison of the mean distances of Lamprigera spp. larvae to the nearest street lamps
211
when they were switched on (1900 – 2200 hrs, N = 41) and switched off (2201 hrs – 0100 hrs, N
212
= 123).
213
Fig. 3. Frequencies at which Lamprigera larvae were located at different ranges of light intensity
214
when street lamps were illuminated at night. Larvae were less likely to use areas where light
215
intensity exceeded 3 lux.
216
Fig. 4. Changes in larval distance to the base of street lamps with time after street lamps were
217
turned off at 22:00 hrs. Distances of larvae to street lamps declined slightly with time, but the
218
difference was not significant.
219
Fig. 5. Percentages of larvae located on and off paved trails when street lights were on versus
220
off. Street lamps were positioned to radiate the maximum light on paved trails for human
221
pedestrians. Larvae were more likely to be seen off paved trails overall, but used paved trails less
222
than expected when street lamps were on.
223 224 225
Title: Effects of artificial light on the larvae of the firefly Lamprigera sp. in an urban city park, Peninsular Malaysia.
226
Authors: Samantha Wanjiru Mbuguaa, Choong Hay Wongb, Shyamala Ratnayekea*
227 228
aDepartment
229 230
bMalaysian
of Biological Sciences, Sunway University, Bandar Sunway, Selangor DE 47500,
Malaysia Nature Society, JKR641, Jalan Kelantan Bukit Persekutuan, 50480 Kuala Lumpur,
Malaysia
231 232
*Corresponding
authors
233 234
Email addresses: [email protected] (S. W. Mbugua), [email protected] (C. H. Wong), [email protected] (S. Ratnayeke)
235 236
Abstract
237
246
Firefly populations are threatened globally by habitat alteration, pesticide use, and anthropogenic sources of light. Lamprigera fireflies were recently reported at an urban city park in Kuala Lumpur, Peninsular Malaysia. Here we report on the responses of Lamprigera larvae to artificial light from street lamps on paved park trails. Larvae were located farther from artificial light sources when street lamps were illuminated than when they were not, and mostly where light intensities were lowest, off park trails. Larvae that were located within the direct field of illumination tended to be immobile, whereas, when street lamps were turned off, they actively travelled paved trails. Larvae positioned directly in the path of downwelling light from street lamps at dusk may therefore experience an effectively longer diurnal period, limited time for active foraging, and greater exposure to pedestrian traffic.
247
Keywords: Artificial light, street lamps, mobility, light intensity, light disturbance.
238 239 240 241 242 243 244 245
248 249 250
We studied responses of Lamprigera larvae to artificial light from street lamps
251
Larvae were active only at night
252
Larvae were farther from street lamps when they were on
253
Larvae within areas of intense artificial light were usually immobile
254 255
256
Figure Captions
257
Fig. 1. Dorsal (A) and dorso-lateral (B) views of the larva and adult female (C; not to scale) of
258
the Lamprigera firefly at Taman Persekutuan Bukit Kiara (Federal Park), Kuala Lumpur,
259
Malaysia. Red arrows in B denote position of larval eyes. Adult females of this genus are
260
apterous or flightless. Lee Sang Soon contributed photographs A and B.
261
Fig. 2. A comparison of the mean distances of Lamprigera spp. larvae to the nearest street lamps
262
when they were switched on (1900 – 2200 hrs, N = 41) and switched off (2201 hrs – 0100 hrs, N
263
= 123).
264
Fig. 3. Frequencies at which Lamprigera larvae were located at different ranges of light intensity
265
when street lamps were illuminated at night. Larvae were less likely to use areas where light
266
intensity exceeded 3 lux.
267
Fig. 4. Changes in larval distance to the base of street lamps with time after street lamps were
268
turned off at 22:00 hrs. Distances of larvae to street lamps declined slightly with time, but the
269
difference was not significant.
270
Fig. 5. Percentages of larvae located on and off paved trails when street lights were on versus
271
off. Street lamps were positioned to radiate the maximum light on paved trails for human
272
pedestrians. Larvae were more likely to be seen off paved trails overall, but used paved trails less
273
than expected when street lamps were on.
274 275