Ecological Entomology (2015), 40, 187–198 DOI: 10.1111/een.

12174

INVITED REVIEW

Pollination by nocturnal Lepidoptera, and the effects

of light pollution: a review
C A L L U M J . M A C G R E G O R, 1,2,3 M I C H A E L J . O . P O C O C K , 2
R I C H A R D F O X 3 and D A R R E N M . E V A N S 1 1 School of Biological, Biomedical and
Environmental Sciences, University of Hull, Hull, U.K., 2 Centre for Ecology & Hydrology, Wallingford, U.K. and 3 Butterfly
Conservation, Wareham, U.K.

Abstract. 1. Moths (Lepidoptera) are the major nocturnal pollinators of flowers.

However, their importance and contribution to the provision of pollination ecosystem
services may have been under-appreciated. Evidence was identified that moths are
important pollinators of a diverse range of plant species in diverse ecosystems across
the world.
2. Moth populations are known to be undergoing significant declines in several
European countries. Among the potential drivers of this decline is increasing light
pollution. The known and possible effects of artificial night lighting upon moths were
reviewed, and suggest how artificial night lighting might in turn affect the provision of
pollination by moths. The need for studies of the effects of artificial night lighting upon
whole communities of moths was highlighted.
3. An ecological network approach is one valuable method to consider the effects of
artificial night lighting upon the provision of pollination by moths, as it provides useful
insights into ecosystem functioning and stability, and may help elucidate the indirect
effects of artificial light upon communities of moths and the plants they pollinate.
4. It was concluded that nocturnal pollination is an ecosystem process that may
potentially be disrupted by increasing light pollution, although the nature of this
disruption remains to be tested.
Key words. Agro-ecosystems, artificial night lighting, ecological networks, ecosystem
services, flowering plants, food-webs, moths, population declines.

Introduction ignoring nocturnal insects, many of which have also undergone

significant declines. In Great Britain, two-thirds of widespread
Pollinating insects have been undergoing significant declines larger moth species populations declined over a 40-year period
for several decades in many parts of the world (Williams, (Fox et al., 2013), with probable detrimental cascading effects
1982; Potts et al., 2010; Carvalheiro et al., 2013). This is of on ecosystem functioning: the nature of these is considered
concern because pollination represents a critical ecosystem a priority, policy-relevant question (Sutherland et al., 2006).
service (Costanza et al., 1997; Ollerton et al., 2011; Garibaldi Recent work suggests that nocturnal moths (Lepidoptera) may
et al., 2013), and declines in pollinators have been linked with perform an important, although often overlooked, functional
declines in the plants that they interact with (Biesmeijer et al., role as plant pollinators (Philipp et al., 2006; Devoto et al.,
2006; Pauw, 2007; Potts et al., 2010). However, most studies 2011; LeCroy et al., 2013), but little is known about the scale
to date have focused on diurnal pollinating insects, largely and importance of nocturnal pollination services. Here, we
review the scientific literature for evidence of the importance of
Correspondence: Callum J. Macgregor, School of Biological, nocturnal Lepidoptera (moths) as plant pollinators.
Biomedical and Environmental Sciences, University of Hull, Nocturnal insect pollinators, including moths, face many
Hardy Building, Cottingham Road, Hull HU6 7RX, U.K. E-mail: of the same threats as diurnal pollinators, including habi-
[email protected] tat fragmentation, climate change, and agrochemical use

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society 187
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited.
188 Callum J. Macgregor et al.

Fig. 1. An illustrative temperate grassland network combining diurnal and nocturnal pollination. Combined networks may reveal the extent of
redundancy and complementarity of pollination interactions in ecosystems. Some apparently specialist plants in diurnal networks may be generalist
with nocturnal visitors included. Thus, nocturnal visitors may provide redundancy to plants pollinated by diurnal visitors, and vice versa. Nocturnal
interactions are derived from Table S1.2, Appendix S2 and diurnal interactions from Pocock et al. (2012). Nodes represent species: white = diurnal
insects, black = nocturnal insects, grey = plants. Pollinators (from left): hoverfly (Diptera), leaf-cutter bee (Hymenoptera), butterfly (Lepidoptera),
bumblebee (Hymenoptera), noctuid moth, pyralid moth, sphingid moth (all Lepidoptera); plants (from left): Ranunculus sp. (Ranunculaceae),
Jacobaea vulgaris (Asteraceae), Trifolium sp. (Fabaceae), Rubus sp. (Rosaceae), Lamium sp. (Lamiaceae), Cirsium sp. (Asteraceae), Silene
latifolia (Caryophyllaceae), Lonicera sp. (Caprifoliaceae), Gymnadenia conopsea (Orchidaceae). Links represent hypothetical pollination interactions:
solid = diurnal, dashed = nocturnal. Drawings of pollinators and plants are for illustration only and may not precisely represent the named plant or
animal. Drawings are used under license from ClipArt ETC (see Appendix S1 for full acknowledgements).

(Fox et al., 2014). They may also be affected by increasing To determine the importance of moths as providers of noc-
light pollution (Hölker et al., 2010a), but the effects of artificial turnal pollination services, and which plants are pollinated,
night lighting on nocturnal pollinator communities have not we searched ISI Web of Knowledge for papers containing the
yet been established. We examine how the known effects of terms ‘moth’ and ‘pollinat*’ (30 January 2014) and searched
artificial light upon moths may potentially affect pollination the bibliography of each relevant publication for further cita-
processes. We also consider how recent advances in network tions. Any paper demonstrating the existence of a moth–plant
ecology can be used to examine the impacts of light pollution pollination interaction or providing evidence for such an inter-
on moth communities and their interactions with plants. action was considered relevant and included in the review.
Levels of evidence supporting pollination interactions var-
ied from observed flower visitation alone to proven depen-
Nocturnal pollination
dence of the flower on moths for pollination (Table 1). Eight
The experimental methods used in the majority of field studies studies only inferred moth pollination from floral characteristics
of plant–pollinator interactions involve observations of insect and did not present further evidence. While a high proportion
visitors to flowers. Such observations almost always take place of flower visitors at any particular flower species may not be
during daylight hours (e.g. Forup et al., 2008; Bosch et al., 2009; effective pollinators (King et al., 2013), flower visitation or
Popic et al., 2013), because conducting surveys in the dark is pollen transfer by insects is frequently used as a proxy for
difficult (Martinell et al., 2010). However, to fully understand insect-pollination. Therefore, for simplicity, we hereafter use
plant–pollinator networks, we must also understand the role the terms ‘pollination’ and ‘pollinator’ where there was rea-
played by nocturnal pollinators (Fig. 1). In addition to some bats sonable evidence that moths acted as pollinators, although we
(Chiroptera), beetles (Coleoptera), and flies (Diptera), moths are note that in many cases pollination was not strictly proven.
important nocturnal pollinators (Willmer, 2011); in particular, Using this method, we identified 168 studies from between 1971
nectarivorous species from the families Sphingidae, Noctuidae, and 2013 detailing examples of nocturnal moths involved in
and Geometridae (Winfree et al., 2011) and probably also the pollination (this search was comprehensive, but we recognise
newly defined Erebidae (LeCroy et al., 2013). that some additional published examples may exist).

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
 Moth pollination and light pollution 189

Table 1. Types of evidence for moth pollination given by studies species Elaeis guineensis Jacq. oil palm (Arecaceae), visited by
reviewed (see Table S1.2, Appendix S2). large numbers of moths in the genus Pyroderces (Cosmopterigi-
dae; Syed, 1979). These observed patterns may be a function
No.
of both real effects and bias in recorder effort, so we treat them
Evidence Types of evidence studies
with caution.
Only flower visitation VF, VO, VR, VT 52 Traditionally, pollination by moths has been subdivided into
recorded two ‘pollination syndromes’ (Willmer, 2011): sphingophily
Flower visitation and moths C + (VF, VO, VR, VT) 11 (pollination by hovering moths of the Sphingidae) and pha-
observed making contact laenophily (pollination by settling moths of other families). The
with floral reproductive
best-known examples of moth pollination are of sphingophilous
organs
plants (e.g. Wasserthal, 1997). To examine if this has led to a
Only pollen found on moths P 15
Flower visitation recorded P + (VF, VO, VR, VT) 49 bias towards sphingophily in studies of moth pollination, we
and pollen found on moths categorised all studies in Table S1.2, Appendix S2 according
Flower visitation recorded (VF, VO, VR, VT) + X 9 to whether they made any explicit or implicit prediction of
with other additional sphingophily. In general, we did not find evidence of bias
evidence towards sphingophily leading to other pollination interactions
Pollen found on moths with P+X 2 being overlooked. Fifty-six studies (35% of those reviewed)
other additional evidence made a prediction of sphingophily. Of these, 53 (95%) found
Flower visitation and pollen P + (VF, VO, VR, VT) + X 8 Sphingidae and 18 (32%) found non-sphingid moths to be pol-
found on moths with other
linators, even although the experimental methods in all but two
additional evidence
studies were sufficient to detect both sphingid and non-sphingid
Other X 4
Only inferred from floral I 8 pollinators. From the 103 studies not predicting sphingophily,
syndrome 82 (80%) found non-sphingid moths and 50 (49%) found
Unspecified/unknown U 5 Sphingidae to be pollinators; the experimental methods in all
but nine were sufficient to detect both sphingid and non-sphingid
In column 2: C = contact with anthers and/or stigmas observed, pollinators (Table S2, Appendix S2).
D = pollen deposited on stigmas and/or removed from anthers,
Moths primarily visit flowers to obtain nectar, which is an
E = plants pollinated when experimentally exposed only to visits by
moths, I = inferred from pollination syndrome, P = pollen present on
energy-rich food source and the main adult food source in
captured moths, S = moth scales or hairs present on stigmas, VF = flower the majority of moth species that feed as adults (Willmer,
visitation determined by fluorescent markers transferred by visiting 2011). Several studies have also documented moths acting as
moths, VO = flower visitation determined by observations, VR = flower pollinating seed parasites (Table S1.3, Appendix S2). In these
visitation determined by video recordings, VT = flower visitation deter- specialised interactions, moths both pollinate and lay eggs in
mined by flower-visitor trapping, U = unspecified/unknown; X = any flowers, so providing a food supply for their larvae, which feed
combination of C, D, E, and S. on developing seedheads.
Pollination by moths may be an advantageous strategy for
Fourteen of these studies examined complete pollinator plants in some examples. Several studies evaluate aspects of
communities, finding moths to be of general importance to pollination in generalist plants pollinated both by moths (both
pollination in a variety of ecosystems (Table S1.1, Appendix Sphingidae and other families) and diurnal pollinators; for
S2), including tropical rainforest and savannah, temperate conif- example, Lonicera japonica Thunb. (Caprifoliaceae; Miyake &
erous forest and meadow, and oceanic islands, and including Yahara, 1998), Asclepias spp. (Apocynaceae; Bertin & Will-
examples from all continents except Antarctica. In several stud- son, 1980; Morse & Fritz, 1983; Jennersten & Morse, 1991)
ies, moths were considered to be second in importance only to and Silene spp. (Caryophyllaceae; Young, 2002; Barthelmess
bees, in terms of pollination provision (Bawa et al., 1985; Kato et al., 2006). Compared with diurnal pollinators, the moths in
& Kawakita, 2004; Ramirez, 2004; Chamorro et al., 2012). these examples provided benefits including: greater interpop-
Moth pollination was important for a wide range of plant ulation gene flow, shown by movement of genetic markers
species. We found representatives of 75 different plant families between experimental populations of plants (Barthelmess et al.,
(Table 2), including 289 species and some wider taxa, reported 2006); longer-distance dispersal of dye-marked pollen (Miyake
to be partially or exclusively pollinated by moths (Table S1.2, & Yahara, 1998; Young, 2002); higher quality pollination, caus-
Appendix S2) of 21 families (Table S3, Appendix S2). The ing equal or greater seed set in spite of transferring fewer pollinia
majority of plants were angiosperms; the one exception was (Bertin & Willson, 1980; Jennersten & Morse, 1991; but see
the gymnosperm Gnetum gnemon Linne var. tenerum Markgraf Morse & Fritz, 1983); and more efficient pollination, having
(Gnetaceae), reportedly pollinated by moths of Geometridae a lower ratio of pollen removed to pollen deposited after vis-
and Pyralidae (Kato et al., 1995). Many species within the its by single pollinators (Miyake & Yahara, 1998). In the latter
angiosperms were dicotyledons, especially from the orders example, moths visiting L. japonica were thought to be more
Caryophyllales, Ericales, Gentianales, and Lamiales, but efficient pollinators than bees because the latter actively col-
moth-pollinated plants in the monocotyledons included many in lect pollen to provision their larvae, and so must remove sub-
the order Asparagales (including Orchidaceae, Amaryllidaceae, stantially more pollen than moths for the same level of pollen
Asparagaceae, and others), and the economically important deposition to occur (Miyake & Yahara, 1999). As a result,

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
190 Callum J. Macgregor et al.

Table 2. Studies of moth-pollinated plants by family (see Table S1.2, Appendix S2).

No. known No. known

moth-pollinated Known pollinating moth-pollinated Known pollinating
Plant family species or wider taxa moth families Plant family species or wider taxa moth families

Adoxaceae 1 N Liliaceae 4 G, N, P, S
Amaranthaceae 1 – Linaceae 1 –
Amaryllidaceae 10 E, N, S Loasaceae 1 S
Anacardiaceae 1 – Loganiaceae 2 –
Apiaceae 1 – Malvaceae 2 Ct, E, G, N, P, Se, S, U
Apocynaceae 20 E, G, N, P, S, T Meliaceae 1 S
Arecaceae 1 C Myrtaceae 2 Ct, S
Asparagaceae 7 N, Pr, S Nepenthaceae 1 –
Asteraceae 13 G, N, P, S Nyctaginaceae 5 N, S
Balsaminaceae 2 S Oleaceae 3 S
Bignoniaceae 3 E, G, L, N, S Onagraceae 8 E, G, N, P, S
Boraginaceae 4 N, P, S Orchidaceae 45 G, N, Pr, Pt, P, Se, S, T
Brassicaceae 3 S Orobanchaceae 2 S
Cactaceae 7 G, N, P, Sa, S Passifloraceae 2 S
Capparaceae 1 P Phrymaceae 1 S
Caprifoliaceae 3 N, S Phyllanthaceae 10 Ge, Gr
Caricaceae 1 – Plantaginaceae 1 –
Caryocaraceae 1 S Polemoniaceae 1 S
Caryophyllaceae 12 Cr, G, N, P, S Polygonaceae 1 –
Cleomaceae 1 S Primulaceae 2 –
Convulvulaceae 4 S Proteaceae 2 S
Crassulaceae 1 G Ranunculaceae 5 S
Cucurbitaceae 1 N, S Rhamnaceae 1 –
Dipterocarpaceae 2 G, N, S Rosaceae 2 –
Ebenaceae 1 – Rubiaceae 16 Ct, N, S
Ericaceae 4 G, N, P, S Rutaceae 1 G
Escalloniaceae 1 G Santalaceae 2 –
Euphorbiaceae 4 S Sapotaceae 2 –
Fabaceae 12 E, G, N, P, S, U Saxifragaceae 3 Pr
Geraniaceae 1 – Scrophulariaceae 2 G, N, P, T
Gesneriaceae 1 – Solanaceae 6 S
Gnetaceae 1 G, P Thymelaeaceae 8 E, G, L, N, No, P, Th
Hyacinthaceae 1 N Urticaceae 1 –
Hypericaceae 1 N Verbenaceae 3 P, S
Iridaceae 3 G, N, S Violaceae 1 S
Lamiaceae 2 S Vochysiaceae 5 S
Lecythidaceae 1 Gl Winteraceae 2 M
Lentibulariaceae 1 N, P, S, U – – –

In column 2, ‘known’ moth-pollinated taxa are those identified in this review as having evidence of being moth-pollinated; ‘wider taxa’ includes any
named group at a hierarchical level above species and below family. In column 3: C = Cosmopterigidae, Cr = Crambidae, Ct = Ctenuchidae,
E = Erebidae, Ge = Gelechiidae, G = Geometridae, Gl = Glyphipterigidae, Gr = Gracillariidae, L = Lasiocampidae, M = Micropterigidae,
N = Noctuidae, No = Nolidae, Pr = Prodoxidae, Pt = Pterophoridae, P = Pyralidae, Sa = Saturniidae, Se = Sesiidae, S = Sphingidae, Th = Thyrididae,
T = Tortricidae, U = Uranidae.

moth-pollinated plants could perhaps invest fewer resources into Artificial light as a driver of environmental change
producing pollen without compromising reproductive success
(Cruden, 1973); however, analysis of pollen–ovule ratios for There are many drivers of environmental change, but artificial
diurnally and nocturnally pollinated members of Caryophyl- night lighting is one which is uniquely important for noctur-
laceae does not support this (Jürgens et al., 2002). nal organisms, through direct interaction with a light source
The literature, therefore, contains numerous examples of such as a streetlamp, increased background illumination at night,
moths serving as pollinators which, in many cases, are of con- and altered perception of photoperiod (Hölker et al., 2010b;
siderable importance to individual species and to communities. Lyytimäki, 2013; Lewanzik & Voigt, 2014). Light pollution has
A diverse selection of plant taxa in an equally wide range of increased considerably and continues to increase worldwide,
ecosystems benefit from pollination by moths. It is important to often associated with urban development (Cinzano et al., 2001;
consider how environmental change may threaten this ecosys- Bruce-White & Shardlow, 2011), although levels may be declin-
tem service. ing in some economically developed regions (Bennie et al.,

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
 Moth pollination and light pollution 191

2014). The predominant types of artificial lighting in use are also females (Garris & Snyder, 2010), but it is not clear if this is due
changing; lights emitting a broader spectrum of wavelengths to stronger male attraction to lights, or males being more active
are increasingly favoured because they facilitate human discern- and therefore more likely to move into the zone of influence of
ment of colours at night and, in the case of light-emitting diodes a given light (Altermatt et al., 2009).
(LEDs), are more energy-efficient (Bruce-White & Shardlow, Aside from flight-to-light behaviour, moths may be further
2011; Gaston et al., 2012). affected by artificial night lighting through other mechanisms,
Artificial night lighting, even at low levels, exerts an influence related to direct interaction with lights, increased ambient light
at every level of biological organisation (Gaston et al., 2013), at night, and locally altered perception of photoperiods in the
from cell (Navara & Nelson, 2007) to organism (Longcore & vicinity of artificial lights. Contact with hot components of
Rich, 2004) and community (Davies et al., 2012). However, lamps or radiant energy from bright lights can kill insects or
little is currently known about the effects of light pollution on damage their wings, legs, and antennae (Eisenbeis, 2006; Frank,
species population dynamics, whole communities, and networks 2006). Insects killed by light-baited electric traps, primarily
of interacting species, or ecosystem functioning. targeting biting Diptera, contain a high proportion of nocturnal
Long-term declines in populations and distributions of Lepidoptera (Frick & Tallamy, 1996).
many moth species have been found in Great Britain (Conrad
et al., 2004, 2006; Fox et al., 2011, 2013), the Netherlands
Reproduction
(Groenendijk & Ellis, 2011), and Finland (Mattila et al., 2006,
2008). Habitat degradation and climate change are likely drivers Reproductive success of moths could also be negatively
of these declines (Fox et al., 2014), as with diurnal pollinators affected by artificial night lighting. Low levels of artificial light
(Potts et al., 2010); however, artificial night lighting has also inhibited the release of sex pheromones by female moths of a
been proposed as a potential contributing factor (Fox, 2013; Geometridae species (Sower et al., 1970). Artificial light can
Fox et al., 2013). Conrad et al. (2006) found no significant suppress oviposition (Nemec, 1969) or act as an ecological trap,
correlation between a change in light pollution and a change in causing females to lay eggs at an unusually high density and/or
light-trap catches from 1992 and 2000, but short-term trends in in unsuitable locations near to lights (Pfrimmer et al., 1955;
moth (and other insect) populations can be difficult to detect, as Brown, 1984), either of which could increase larval competition
large inter-annual fluctuations are normal (Conrad et al., 2004). for limited food resources.
Below, we describe a range of mechanisms by which artificial Artificial light may also have an effect on larvae, which are
night lighting could impact negatively upon moths. Many such nocturnal in many Lepidopteran species, including some that are
impacts are not empirically proven. Therefore, we describe first diurnal as adults (butterflies and day-flying moths). Even at a low
the well-established mechanisms, followed by those unproven, intensity, light caused reductions in age and mass at pupation
but for which some evidence exists. Even where negative in males and inhibited diapause in both sexes of a Noctuidae
impacts have been demonstrated, their effects at the population species in the laboratory (van Geffen et al., 2014). However, few
level are mostly unknown. studies have investigated the effects of artificial night lighting on
Lepidopteran larvae.

Established effects of artificial light on moths Predation

Individual moths are certainly affected by artificial night light- Predators of moths have been observed to hunt at artifi-
ing, famously appearing to be attracted to artificial lights, some- cial lights, exploiting above-average prey densities caused by
times in huge numbers (Howe, 1959). Numerous theories have flight-to-light behaviour (Frank, 2006). This includes both active
been put forward to explain flight-to-light behaviour (Robin- hunters, such as bats (Rydell, 1992) and predatory insects (War-
son & Robinson, 1950; Mazokhin-Porshnyakov, 1961; Calla- ren, 1990), and sit-and-wait predators, such as spiders (Heil-
han, 1965; Hsiao, 1973; Sotthibandhu & Baker, 1979; Hamdorf ing, 1999), reptiles, and amphibians (Henderson & Powell,
& Höglund, 1981), although the debate is inconclusive. Never- 2001). Artificial light also interferes with the anti-bat defensive
theless, this observation has led to the popularity of using behaviour of moths, increasing their vulnerability to predation
light-baited traps to survey many families of moths. (Svensson & Rydell, 1998; Acharya & Fenton, 1999).
The extent to which moths are attracted to light varies accord-
ing to a number of factors. It has been recognised for many
years that shorter wavelengths are, in general, more attractive Possible further effects of artificial light on moths
to moths (Frank, 2006, and references therein); attractiveness
In addition to the known mechanisms described above, a number
appears to peak around wavelengths of 400 nm (violet light;
of other mechanisms have the potential to affect moths but have
Cowan & Gries, 2009). The degree of attraction and preferred
not yet been conclusively demonstrated.
wavelengths both vary between moth taxa (Merckx & Slade,
2014); typically, larger-bodied moths with larger eyes are more
likely to be attracted to light dominated by smaller wavelengths Reproduction
(van Langevelde et al., 2011; Somers-Yeates et al., 2013). Vari-
ation also appears to exist between sexes; males of some species Changes in photoperiod disrupted the pheromone release
are significantly more likely to be recorded at light traps than behaviour of females of a Pyralidae species (Fatzinger, 1973),

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
192 Callum J. Macgregor et al.

which could disrupt mating. Competition in male moths between moths, as moths orient themselves to flowers by a combination
light traps and pheromone traps (Delisle et al., 1998) sug- of olfactory and visual cues (Raguso & Willis, 2005) including
gests that artificial lighting could distract males from female UV-reflecting markers on flowers (Barth, 1985). The spectral
pheromone signals and thus reduce mating frequency. More content of artificial night lighting will therefore determine its
severely, radiant energy from bright lights can sterilise other effect upon flower-visiting moths (Davies et al., 2013): UV-rich
insects in the laboratory (Riordan, 1964; Eisenbeis, 2006); this lighting (e.g. from mercury vapour lights) could accentuate these
could occur with moths in the wild. Artificial lights have been nectar guides, whereas UV-poor lighting (e.g. from low-pressure
observed to divert dispersing or migrating moths to locations sodium lights), by illuminating other parts of the nocturnal envir-
that are unsuitable for breeding (Frank, 2006, and references onment relatively more brightly, could cause nectar guides to
therein), potentially creating an ecological trap. stand out less clearly (Frank, 2006).
A reduction of the dark scotophase of the photoperiod pre-
vented diapause in the larval stage of a Tortricidae species in the
laboratory (Berlinger & Ankersmit, 1976); however, this result
could not be replicated in field trials. In addition, moth larvae Moths and pollination: an ecological network
may be attracted to artificial lights in much the same way as approach
adults (Gillett & Gardner, 2009).
The studies above considered the direct effects of artificial light
upon moths, mostly at the level of the individual. Whether artifi-
Predation cial night lighting, through these effects, is a contributing factor
in declines in moth populations remains a key research question.
Artificial light may also increase the risk of predation by dis- It is also necessary to consider the indirect effects of artificial
rupting crypsis, both by causing moths to rest in unsuitable light mediated by moth pollination, as can be demonstrated with
locations where their wing patterns are an ineffective disguise, an ecological network approach. Ecological networks describe
and by concentrating moths in a small area, assisting predators the structure of communities as the occurrence (and frequency)
in establishing a search image of cryptic wing patterns (Frank, of interactions between species, such as plants and pollinators
2006). Similarly, repeat exposure can habituate predators to (Montoya et al., 2006; Bascompte, 2007). From descriptions of
stimuli that elicit startle reactions, such as patterned hindwings the network’s structure, its function can be inferred (Tylianakis
or bodies (Schlenoff, 1985; Ingalls, 1993); highly visible aggre- et al., 2010); for example, its robustness to perturbations such
gations of moths around lights could accelerate the habituation as species extinction and their cascading effects (Bascompte,
process (Frank, 2006). 2009; Ings et al., 2009; Evans et al., 2013). It has been demon-
strated that drivers of environmental change, such as climate
change, can alter the composition and balance of networks
Vision (Tylianakis et al., 2008), including plant–pollinator networks
Artificial light affects the sensitivity of the compound eyes (Rathke & Jules, 1993; Memmott et al., 2007). Removal of pol-
of moths (Frank, 2006). Screening pigment reduces ocular linator species can cause plant species diversity to suffer (Mem-
sensitivity within 23 min of exposure to light (Hamdorf & mott et al., 2004; Fontaine et al., 2006), while loss of plants can
Höglund, 1981); the return to full ocular sensitivity is far slower, likewise affect pollinators (Wallis De Vries et al., 2012).
taking around 30 min (Bernhard & Ottoson, 1960). To what Two attributes of networks are particularly important. First,
extent these effects may be exerted by exposure to artificial many pollinator networks have a nested structure, in which
lights in natural settings is unclear. However, moths attracted to specialist species (with few connections in the network) tend
a light will often rest on vegetation or the ground for a period of to interact with generalists (with many connections) more fre-
time, sometimes before even reaching the light (Hartstack et al., quently than with other specialists (Dicks et al., 2002; Bas-
1968; Hsiao, 1973); this behaviour could represent a period of compte et al., 2003). Nested systems have high tolerance to the
readjustment to full ocular sensitivity. random loss of species from the community but are sensitive to
In addition to compound eyes, most insects (including moths) the removal of certain highly connected species (Solé & Mon-
have simple eyes (dorsal ocelli) that are sensitive to changes toya, 2001; Memmott et al., 2004). Second, these systems are
in light intensity (Mizunami, 1995), and appear to have a role also modular, in which sets of species within modules interact
in timing flight initiation at dusk in moths (Eaton et al., 1983). strongly with each other; these modules are akin to pollination
It is possible that artificial night lighting could delay or even syndromes (Olesen et al., 2007), and increase overall robust-
prevent the onset of nocturnal activity. While this effect is likely ness because impacts cascade less quickly between modules and
to be localised to the immediate vicinity of light sources, it could through the whole system. Some modules are as a result of close
negatively affect moth fitness (and hence population growth) and co-evolutionary relationships; in extreme examples, plants are
nocturnal pollination. entirely reliant on a single or few species of moth [eg. Oxyan-
The visual capacity of moths could also be indirectly affected thus pyriformis (Hochst.) Skeels (Johnson et al., 2004)]. In such
by artificial night lighting altering the spectrum of back- cases, minor disruption of the pollinator will directly impact the
ground illumination. Ultraviolet (UV) radiation (10–400 nm), reproductive success of the plant (Pauw, 2007). The modules
predominantly at longer wavelengths close to visible light themselves may be nested within the whole system, and species
(Eguchi et al., 1982), is particularly important to pollinating will often be nested within modules.

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
 Moth pollination and light pollution 193

Fig. 2. Possible scenarios for change in plant–moth pollination networks as a result of artificial night lighting, with predictions for effects on local
flower-visitation activity by moths. In network representations, nodes represent species (lower = flowering plants, upper = moths) and links represent
pollination interactions. Node width represents relative species abundance and link thickness represents interaction strength. Crosses indicate disruption
of behaviour.

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
194 Callum J. Macgregor et al.

Are moths pollinators of a wide Is increasing artificial light a Does artificial light alter the
range of plants or just specialists causal factor in the decline of interactions of moths with other
in a moth-pollination syndrome? moth populations? organisms?

Are moths important and What are the community-

valuable providers of level effects of artificial light
pollination services? on moths?

Are moth-pollinated plants of

Does artificial light alter the
value, economically or otherwise,
composition of moth
to humanity?
assemblages?
Does artificial light affect plant–
moth pollinator interactions?

Does artificial light affect the

pollination ecosystem service?

Fig. 3. Future research directions raised in this review.

Most studies of plant–pollinator networks to date have 2013), leading to some interactions being more strongly affected
focused on diurnal interactions. Two exceptions consider- than others (Fig. 2: preferential disruption effect). If reproduc-
ing nocturnal plant–pollinator networks are Devoto et al. tion is affected, some moth species may decline in abundance
(2011) and Banza (2011); these authors identified nocturnal or go extinct, leading to further loss of interactions. Therefore,
moth–flower interactions by sampling pollen on captured the effects of increasing artificial light may be positive for some
moths. Combining nocturnal pollination networks with diurnal moth or plant species and negative for others in any given com-
ones could lead to increased modularity (if there are distinct munity, leading to cascading changes in the system that are dif-
sets of flowers visited by diurnal and nocturnal pollinators), ficult to predict prior to empirical, experimental research.
such that the effects of environmental change (e.g. artificial
night lighting) could be substantial in one part of the network Discussion
but not cascade through the whole network. It could also lead
to increased redundancy (if flowers share diurnal and nocturnal Future research directions
pollinators), such that the plants in the network may be robust to
the disruption of one set of pollinators (e.g. moths). Testing for We believe that our findings in this review highlight a number
differences in the structure of plant–moth pollinator networks of key priorities for future research (Fig. 3). While we have
between unlit and artificially lit sites will begin to empirically described evidence that moths are pollinators of a diverse
reveal the functional impact of artificial night lighting on wider range of plant species, the extent of their role as pollinators
communities through indirect, as well as direct, effects. in maintaining botanical diversity, in agro-ecosystems, and
especially of commercially valuable crops demands attention.
The effects of artificial night lighting on moths, too, should
be investigated further. Many of the individual-level effects
Potential effects of artificial light on moth pollination
summarised above have not been empirically demonstrated
A variety of changes in moth abundance, composition of moth to occur under natural conditions. Moreover, there are no
assemblages, and moth behaviour are all possible results of arti- published studies into the community-level effects of artificial
night lighting on moths; this is a major research gap (Fox, 2013;
ficial lighting at night, but the overall effect on the whole com-
Gaston et al., 2013). The impacts of lighting on plant–moth
munity via disruption of pollination remains to be tested (Fig. 2).
pollination networks are difficult to predict (Fig. 2) and also
Moths may be drawn in towards a light from several metres away
require empirical testing. It is worth noting that moths are a food
(Baker & Sadovy, 1978; Truxa & Fiedler, 2012; van Grunsven
source for many other organisms including birds and bats (Fox,
et al., 2014); this might alter local moth abundance and the com-
2013); therefore, a similar approach with trophic networks may
position of moth assemblages both in the vicinity of lights, and
also be worthwhile.
in the source habitats from which attracted moths are drawn
(Fig. 2: concentration and ecological trap effects). Interactions
could also be weakened or lost through behavioural changes in Conclusion
moths, even if their abundance is unchanged (Fig. 2: disruption
effect). The level and nature of disruption might vary between In this review, we show the importance of moths as pollinators
moth species (van Langevelde et al., 2011; Somers-Yeates et al., for a diverse range of plant species in ecosystems worldwide

© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198
 Moth pollination and light pollution 195

and, hence, their role in ecosystem functioning. We discuss the Bascompte, J. (2009) Disentangling the web of life. Science, 325,
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© 2014 The Authors. Ecological Entomology published by John Wiley & Sons Ltd on behalf of Royal Entomological Society
Ecological Entomology, 40, 187–198