Comparative function of blacklight and visual light sources in capturing Harmonia axyridis in the field and laboratory conditions; effect of color polymorphism

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Comparative function of blacklight and visual light sources in capturing Harmonia axyridis in the field and laboratory conditions; effect of color polymorphism

https://doi.org/10.21203/rs.3.rs-2472082/v1

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Light trapping is one of the most popular sampling methods for monitoring pests’ populations in IPM programs. Harmonia axyridis (Coleoptera: Coccinellidae), which is a voracious aphid predator, needs to be monitored for several reasons; e.g. for its function as an invasive alien species newly appeared in many non-native countries. Lots of studies and observations show that this ladybird is significantly attracted to blacklight traps. Two major color morphs of H. axyridis (melanic and nonmelanic) appear with different ratios in different populations. In this study, the outcome of two sampling methods, including light trapping and foliage beating were evaluated in terms of the color morph combination and sex ratio in the field. Also, two types of light sources (blacklight (UV) and visual light LED) were compared in attracting the two color morphs in the laboratory conditions. Field results, where the ladybirds could fly towards the light source, indicated that blacklight trap captures less melanic individuals compare to mercury light trap and foliage beating, while there was no difference between the two latter methods. Also sex ratios were not different among the sampling methods. However, blacklight (UV) and visual light sources did not show any effect on attracting the two morphs in laboratory conditions, where the ladybirds could only walk towards the light sources. Comparing the results from field and laboratory experiments suggest that H. axyridis shows different phototaxic reactions based on its locomotion options.

Asian multicolored ladybird

color polymorphism

blacklight

phototaxis

coccinellidae

Phototaxis is the ability of an organism to move towards or against a light source. This reaction is affected by several factors including the light wavelength as well as the quality and intensity of the light source (Cloyd 2007). When it comes to insects, light wavelength ranged from 330 to 700 nm can be perceived by the animal (Meinertzhagen et al. 1983; Land 1997; Kelber et al. 2003). Insects are not similarly attracted to different light wavelengths (Somers- Yeates et al. 2013; Van Grunsven et al. 2014; Wakefield et al. 2016), with shorter wavelengths including ultraviolet (UV) (< 380 nm) being more attractive than longer wavelengths (e.g. van Langevelde et al. 2011).

Light traps employ phototaxic behavior of insects for a variety of purposes, such as obtaining information on diversity (Thomas and Thomas 1994; Southwood and Henderson 2000; Ramamurthy et al. 2010), geographic ranges, migration patterns (Gregg et al. 1994), population density (Thomas 1989), and controlling populations of agricultural pests in fields (Cantelo et al. 1972; Frank 1988). Among the insect orders, Diptera, Coleoptera, and Lepidoptera are attracted to and captured in light traps the most (Mikkola, 1972; van Grunsven et al. 2014; Wakefield et al. 2016; Owens and lewis 2018). Although the moths include only 7.4–19.9% of the total number of insects species attracted to light, the majority of the studies concerning insects phototaxis have focused on them (Eisenbeis and Hassel 2000; Eisenbeis and Eik, 2010).

However, one shortcoming of light trapping is that not always are the samples collected in an area, representative of the actual combination of individual types in a specific species population. As light traps rely on the disturbance of normal behavior for their functioning, their efficiency is highly subject to variation from insect to insect, from night to night, and from site to site (Southwood 1978; Nalepa 2013). Most of the studies concerning light traps skewed collection have focused on male-female ratio of Lepidopteran insects (e.g., Worth and Muller 1979: Yathom 1981; Levine 1989; Steinbauer 2003; Garris and Snyder 2010; Cheng et al. 2016; Degen et al. 2016; Brehm et al. 2021), reporting less females than males, and less unmated females than mated females (Cheng et al. 2016). For some species, this bias is been attributed to reproductive and mating behaviors (Brehm et al. 2021; Cheng et al. 2016).

Ladybirds (Coccinellidae), as diurnal visual predators (Hodek & Honěk 1996), are also among the insect who are attracted to light sources frequently, mainly to those equipped with blacklight (UV). And among the ladybirds, blacklight traps seem effective in capturing the multicolored Asian ladybird, Harmonia axyridis Pallas, particularly. Lots of studies and observations suggest that this ladybeetle is strongly and consistently attracted to blacklight traps, while presence of other coccinellid species is more sporadic (Koch and Hutchinson 2003; Hesler et al. 2004; Nalepa 2013).

H. axyridis, as an effective aphid predator, is native to central and eastern Asia. However, it is an invasive species with a high dispersal ability, establishing its populations in many areas outside its native origins (Brown et al. 2011; Roy et al. 2016; Camacho-Cervantes et al. 2017). H. axyridis, is a highly polymorphic ladybird, containing specimens with red or orange elytra ground with black spots (non-melanic), and black elytra ground with orange or yellow spots (melanic). Different geographical populations include various proportions of each morph. For instance, while in the USA only 1% of the individuals and even less are melanics (Tedder and Scheafer 1994; Lamana and Miller 1996; Zakharov and Blekhman 2013), in European populations up to 28% of the populations are consisted of melanic individuals (Brown et al. 2008). In Siberia and Baikal region, up to 90% of the population are of the melanic morph (Belyakova 2013). Such polymorphic diversity in a given population is affected by climate differences (Dobzhansky 1924, 1933), seasonal changes (Komai, 1956, Osawa and Nishida, 1992), and unknown factors (Komai et al., 1950).

The first records of multicolored Asian ladybirds in new geographic areas is often subsequent to its capture in blacklight traps (Chapin and Brou 1991; Stanković et al. 2011). These traps also have been used to determine peak activity of H. axyridis in agricultural landscapes (Galvan et al. 2009) and to catch adults in dark, confined spaces inside buildings during the winter aggregation period (e.g., Waldvogel et al. 2003; Kenis et al. 2008).

Although there are a handful of studies concerning genetic, morphological, biological and behavioral differences between color morphs of H. axyridis (e.g. Brakefield and Willmer 1985; Osawa and Nishida, 1992; Seo et al. 2008), their differential reactions against environment stimuli remains relatively unexplored. Being known also as an urban pest, understanding the effect of light sources with different spectral compositions can help us coping with its presence in residential areas. The current study was conducted to examine the hypothesis that blacklight traps attract the two color morphs of H. axyridis differentially.

Field studies

1. Light Traps

Two types of light trap, different in light sources, but similar in the structure, each including two metal cones; the upper one as the traps roof (40 cm diameter and 30 cm height) and the lower as the collecting bucket (35 cm diameter and 30 cm depth), attached by two metal bars, were used to collect H. axyridis during spring and summer.

One trap was equipped with a blacklight tube (Hitachi, BL, 18W) (Fig. 1a), while the other one was illuminated with a mercury vapor bulb (Osram, HWL, 160 W) (Fig. 1b) in the space between the two cones. Beneath each trap, under the collecting bucket, a glass jar charged with 50 ml Ethyl Acetate was fixed in which the insects would fall and get sedated.

Two light traps were installed two meters above the ground, in an open area covered with arboreal, bush, and grass plantation, with no light pollution during the night, located in University of Guilan, Rasht (37.19°N, 49.64°E), Iran.

On two different periods, i.e. one during April and May (spring) and then during July and August (summer) (2021), when the most number of adult ladybirds could be captured (personal observations), the two light traps took turn collecting the specimens every other night. Each light trap collected insects for 20 nights during each sampling period (every other night). The light sources operated during the whole dark hours and then early in the morning the glass jar was detached and transferred to the laboratory in order to separate and count melanic (M) and non-melanic (NM) ladybirds and to determine their sex.

In order to diagnose sex of the individuals, three criteria, described by McCornack et al. (2007), were taken into consideration, including labrum pigmentation, protsternum pigmentation, and the distal margin of 5th visible abdominal sternite.

2. Foliage Beating

Given that foliage beating gives us a more reliable samples of H. axyridis in terms of the variation in individuals within a natural environment (Micheles and Behle 1992), during the periods when light trappings were in operation, the ladybirds were also collected by beating method from plantations of the same area (including plane, cotton wood, oak, flowering quince, etc.). Foliage beatings were done close to the light trapping zone but where the area was not illuminated by lights traps during the night. Beating was repeated 20 times during the two sampling periods. All beatings carried out before 9 a.m. and lasted 20 minutes. Plants’ sticks were beaten above a cloth cone and then collected insects were transferred to the laboratory to count the two morphs of the ladybirds and determine their gender.

Proportion of the melanic morph individuals to total number of H. axyridis captured in light traps during each night, and of each single foliage beating on the following day were compared by ANOVA using SAS software.

Sex ratio data were compared by Chi square procedure by means of SAS software (version 9/1).

Laboratory Studies

2.1 Two-choice experiment

Two PVC tubes (150×15 cm) were attached in a row with a cardboard tube (40×15 cm) in the middle (Fig. 2). The cardboard tube was equipped with a 5 cm diameter opening through which the insects could enter the tunnel. One end of this structure was equipped with a SMD blacklight LED (UV) (10 W, 320–400 nm), while the other end was equipped with a SMD visible light LED (10 W, 400–750 nm). Both light sources would cast light onto the other end of the tube, so that when the insects entered the cardboard space between the two PVC tubes, could receive both light types from same distances. During the experiments, the two ends of the structure were blocked with two pieces of dark thick fabrics in order not to let the room light enter the tubes.

A group of six melanic and six non-melanic ladybirds (collected from the nature and having experienced darkness for three hours in laboratory conditions) were released into the opening of the cardboard tube. Then immediately the opening lid was closed and the two light sources were turned on simultaneously. The insects were given 10 min. time to choose which light source they wanted to approach. The lights were then turned off simultaneously, and the insects attracted to each light source were removed and recorded. Ladybirds that had left the cardboard area were considered as having chosen one light source. This procedure was repeated 15 times in two rounds in which the two light sources replaced each other. Data was analyzed by nonparametric Wilcoxon matched-pairs signed-ranks test using SAS software (version 9.1).

2.2 Non-choice Experiment

In this experiment only one PVC tube (150×15 cm) was used. It was attached to the same cardboard tube as described in the former experiment. The open end of the cardboard tube was blocked and the other end joined the PVC tube making a tunnel towards the light source at the other end of the PVC tube (Fig. 3). Same two sources of light as the former experiment (blacklight LED and visible light LED) were used. Six melanic and six non-melanic ladybirds entered the opening of the cardboard tube, the opening lid was closed, and the light source was turned on immediately. The ladybirds were given 10 min. time to leave the cardboard tube area towards the light source. This was carried out 15 times with each type of light sources on. The ladybirds which had left the cardboard area towards the other end of the tunnel were considered as attracted to the light.

Light trap and foliage sampling

Proportions of melanic specimens of H. axyridis obtained from three sampling methods during two seasons are shown in Fig. 4. Light trap samplings during the spring, gave a total number of 391 (47 M and 344 NM) and 327 (58 M and 269 NM) harlequin ladybirds captured in blacklight and mercury vapor light traps, respectively. Summer light trap samplings also resulted in 328 (35 M and 293 NM) and 261 (41 M and 220 NM) H. axyridis in blacklight and mercury vapor light traps, respectively. Averages of the melanic morph proportion from all single samplings were 0.116756 and 0.1839 (spring samplings) and 0.1048 and 0.1596 (summer samplings) for blacklight and mercury vapor light, respectively.

Foliage beating method resulted in as many as 593 harlequin ladybirds (102 M and 491 NM) and 483 (78 M & 405 NM), in spring and summer, respectively. Mean of melanic proportion captured in each single beating was 0.1808 and 0.1645 for spring and summer samplings, respectively (Fig. 4).

In spring, blacklight trap captured significantly less melanic specimens than non-melanics compared to both mercury vapor light trap (p < 0.0001) and foliage beating method (p < 0.0001), while there was no difference between mercury vapor light traps and foliage beating method (p = 0.941).

Same trend was also observed for summer sampling, so that significantly less melanic specimens than non-melanics were captured in blacklight trap compared to both mercury vapor light trap (p < 0.0001) and foliage beating method (p < 0.0001). There was again no difference between mercury vapor light trap and foliage beating method (p = 0.941).

In all three sampling methods, more melanic specimens were captured during spring compared to the summer (Fig. 4). For blacklight trap, mercury vapor bulb, and foliage beating in spring, 12, 17.7, and 17.2%, of the individuals were of melanic morph, while in the summer, 10.6, 15.7, and 16.1% were of melanic specimens, respectively.

Sex Ratio

Sex ratio (proportion of females) of the specimens collected via different methods, during the two time periods were as follows; during the spring, the sex ratios were 44, 43.3, and 44.3% in the samples collected through blacklight trap, mercury vapor trap, and hand collection, respectively. In summer, and by the same methods, the sex ratios were 40.8, 41.1, and 44.1%, respectively (Fig. 5). According to chi square results there was no difference among the three sampling methods in each season, nor between the two seasons for same sampling methods (x² = 0.23).

Indoor Experiments

In the choice experiment, after 30 replications, when the insects were allowed to choose between the two arms illuminated by blacklight or visible light (Fig. 2), among all the ladybirds who had left the cardboard area, only three insects were attracted to the visual light. Neither them, nor the insects who had not left the cardboard area were taken into consideration for analyses. Since the majority of the ladybirds selected the blacklight source (12 ladybirds in 18 replications out of 30), comparisons were made between the two color morphs who had entered the PVC tube equipped with blacklight source. Consequently, in both rounds of experiments, replacing the light sources location, both color morphs selected blacklight equally (Exact test two-sided p ˂ 0.03).

In the non-choice experiment, where the ladybirds were exposed to only one type of light source in each treatment (Fig. 3), they selected the two light sources equally. In other words, in all replications, all of the ladybirds including both color morphs moved towards the light source regardless of the light type. Consequently, no analytic process was carried out on these set of data.

Studying color morph combination in the populations of a given polymorphic insect is of a great importance. For instance, color polymorphism in H. axyridis is considered as an index for different seasonal (Osawa and Nishida 1992), geographic, and climatic conditions (Dobzhansky 1924, 1933; Komai 1956; Belyakova 2013) in which the population has expanded, and also a consequence of the condition in which the individuals’ immature stage have developed (Michie et al. 2010). So, having a realistic knowledge of populations’ combination in terms of morphological features, can help us understand the context in which the population and the individual have developed. Moreover, it helps us predict the future state of a population in an area, newly invaded by H. axyridis.

During samplings for H. axyridis, blacklight trap arrested less melanic individuals compared to what was observed in the population living on the plants in the same area. There are a couple of studies reporting differential attraction of blacklight for male and female individuals of some species (e.g. Garis and Snyder 2010), nonetheless, this is the first study questioning the ability of blacklight traps in giving a convincing representative of natural populations in terms of the color morph combination.

Although there are a few theories suggested, there are no determined explanation on why insects are attracted to artificial light sources. A popular, but still not fully conclusive and convincing explanation for their flight-to-light behavior is that they fly to a strong light source mistaking it for the moon (Hsiao 1973). When it comes to more specific and detailed differences among individuals of a given species, it is even more difficult to justify the behavior.

In the light spectrum, short wavelengths are strongly attractive to many insects (Barghini and de Medeiros 2012; Mikkola 1972 Wakefield et al. 2016; Owens and Lewis 2018; van Langevelde et al. 2011; Brehm et al. 2021). The capability to perceive the ultraviolet light is a crucial constituent of insect vision and is used for several purposes. For instance, insects use UV light to locate open space. The sun and the sky are the only natural sources of ultraviolet light, and when insects fly from the interior of vegetation towards open space, they seek a UV-bright light gap (Goldsmith 1961; Hu and Stark, 1977). The second important use of UV light occurs while foraging. Some flowers (Frolich 1976; Silberglied 1979), fungi (C. L. Craig, personal observation), and liquids (Schwind 1985) reflect UV light and attract insects searching for food resources, mating, or oviposition sites (Graic and Bernard 1990). Finally, some predatory animals employ this feature to trap their prey. For instance, primitive spiders produce silks that reflect ultraviolet (UV) light, which together with their UV reflecting body, attract flying insects. (Graig and Bernard 1990).

There are a considerable number of studies concerning wavelength spectrum, in which animals’ photo receptors show maximal sensitivity (Kelber et al. 2003). In spite of the similarity of the basic pattern of spectral sensitivity of insect photoreceptors in most insects, there are also differences in the spectral sensitivity (Briscoe and Chittka 2003). Consequently, variation in attraction between different (groups of) insects can be expected (Somers-Yeates et al. 2013). The spectral sensitivity is currently unknown for many orders or only known for a small number of species. Hence, the physiological interpretation of the found patterns is currently impossible (van Grunsven et al. 2014).

Mercury vapor gas light (200–600 nm), as a white light source, emits light in a wider spectrum of wavelength than blacklight does (320–400 nm), covering a wider range of spectrum than most of other artificial light sources. When it comes to different sampling methods for insects, generally, for arboreal species like H. axyridis, foliage beating, compared to blacklights, gives us a better understanding of the population combination in terms of the color morphs and sex ratio. So we can consider its samples as a criteria to which other sampling methods can be compared.

As mentioned earlier, the most studied cases regarding skewed sampling of blacklight traps have focused on moths’ sex ratio. For coccinellids, it was suggested that sampling with blacklight traps could bias documentation of the relative abundance of species in a given area (Koch & Hutchinson 2003; Hesler et al. 2004). Now, according to the results of this study, we can claim that blacklight trap can also cause interspecies biased sampling compared to the actual combination in a population in terms of morphological characteristics. Although there are many studies reporting variation in insects’ spectral sensitivity among different families and different genus of a family (van Grunsven et al. 2014), it was unexpected to observe differential phototaxic reaction within a species, stemmed from a morphological difference.

Regarding the morph differential reaction against blacklight, a number of explanations are possible. For instance, the two morphs might perceive and respond to UV light in different ways. One morph might have a more limited flight range, or some combination of these and other factors might be occurring. Such suppositions have not been studied yet. Similar reaction to black and visual light sources in the indoor experiments, where ladybirds flying ability was limited and they had to walk towards the light sources, shows that the effect of light type appears when the insect has to move a longer distance or when it is able to use its flight ability. So the difference between the two morphs of H. axyridis can also be sought in the difference of the two morphs in perceiving or reacting to environmental stimuli while flying. There are some studies indicating photopreference changes in flies whose flight ability is manipulated, so that they have to walk towards the light sources rather than flying (McEwen 1918; Benzer 1967; Gorostiza 2016). These studies attribute flies’ different phototacic behavior to their less assessment of the environmental conditions, rather than their hypoactivity.

What insects receive as heat energy from light sources, may be another factor making the light source more or less desirable for them. Melanic form of H. axyridis, as the darker morph, absorbs more heat and can reach a higher body temperature than non-melanic forms (Brakefield and Willmer 1985; Trullas et al. 2007). Generally, proportion of the darker morph in the population decreases in the generations living during warmer seasons (Osawa and Nishida 1992) or towards warmer regions (Dobzhansky 1924, 1933; Komai 1956; Belyakova, 2013). In our study also samplings in early spring, resulted in more melanic specimens as compared to the samplings during summer. Darker individuals can reach higher metabolic rate and biological activity (Digby 1955; Lusis 1961; Dixon 1972; Benham et al. 1974; Muggleton et al. 1975; Willmer and Unwin 1981; Brakefield and Willmer 1985; Stewart and Dixon 1989; De Jong et al. 1996; Soares et al. 2011). Such differential effect of heat on the two color morphs, may make them avoid or welcome some types of light sources or spectral light waves when considering the light source as heat source too.

Since most of the studies concerning skewed sampling of blacklight traps have focused on the sex ratio, we decided to study this feature too. Consequently, there was no difference neither among the sampling methods, nor between the seasons in terms of the sex ratio. While sex ratio of our samples ranges from 40.8–44.3%, an earlier study in the same region separated only 36% females in their samplings (Mardani-Talaee et al. 2019). In other studies done in different geographical locations, sex ratio ranged from 41.1–87.5% (Seo et al. 2008; Nedved and Kalushkov 2012; Osawa 2001; Nalepa et al. 1996). Such differences are attributed to the season and place of samplings (Osawa 2001; Seo et al. 2008), air humidity (Nedved and Kalushkov 2012), and male killing microorganisms.

As an urban pest, morph frequency and distribution of H. axiridis should be studied in urban areas with different types of light pollution and between urban areas and non-light-polluted landscapes. While recent increasing urban light pollution may be a driver of the current decline of many nocturnal insects in industrialized countries (Groenendijk and Ellis 2011; Fox et al. 2011; Conrad et al. 2006; Hu and Stark 1980; Fox 2013), urban illumination, may also affect non-nocturnal insects such as ladybirds in terms of the population combination and distribution. Studying morph combinations in the populations living in the areas with or without artificial light pollution can add more information to our current data.

Although according to the results of the current study we cannot suggest any robust explanations for why melanic specimens of H. axiridis are less attracted to blacklight traps, at least we now know that sampling by blacklight traps should be done more cautiously and be supported by data from other methods of sampling in order to have a more realistic estimation.

Funding

This study was funded by the University of Guilan, Iran

Author’s contribution

The first author did the practical experiments and data analyzing and also prepared the main manuscript including the figures, and all authors reviewed the manuscript before submission. Dr. Sahragard, as the supervisor, together with Dr. Hosseini and Dr. Saboori, as the advisors, observed the process of designing the experiments, collecting and analyzing the data, and preparing the manuscript.

Statements and Declarations

The authors declare that they have no conflict of interest and no competing interests.

Barghini A, de Medeiros BAS (2012). UV radiation as an attractor for insects. Leukos 9: 47–56.
Belyakova NA (2013). Polymorphism of the Harlequin Ladybird Harmonia axyridis (Coleoptera, Coccinellidae) Baikal Population. Zoologicheskii Zhurnal 91: 961–966.
Belyakova N (2013). Polymorphism of the harlequin ladybird Harmonia axyridis (Coleoptera, Coccinellidae) Baikal population. Entomological Review 93 (1): 50–55.
Benzer S (1967). Behavioral mutants of drosophila isolated by countercurrent distribution. Proceedings of the National Academy of Sciences of the United States of America. 58, 1112–1119.
Brehm G, Niermann J, Jaimes- Nino LM, Enseling D, Jüstel T, Axmacher JC, Fiedler K (2021). Moths are strongly attracted to ultraviolet and blue radiation. Insect Conservation and Diversity, 14,188–198.
Brakefield PM, Willmer PG (1985). The basis of thermal melanism in the ladybird Adalia bipunctata: Differences in reflectance and thermal properties between the morphs. Heredity 54, 9–14
Brown PMJ, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley LJL (2011b). The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. Biocontrol 56, 623–641
Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A, Hagg T, Kenis M, Klausnitzer BEM, Kovar I, Loomans AJM, Majerus MEN, Nedved O, Pedersen J. Rabitsch W, Roy HE, Ternois V, Zakharov IA, Roy DB (2008a). Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53, 5–21.
Camacho-Cervantes et al. (2017). From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ 5:e3296
Cantelo WW, Smith JS, Baumhover A.H, Stanley JM, Henneberry TJ (1972). Suppression of an isolated population of the Tobacco Hornworm with blacklight traps unbaited or baited with virgin female moths. Environmental Entomology. 1,253–258
Cloyd RA (2007). Phototaxis of fungus gnat, Bradysia sp. nr coprophila (Lintner) (Diptera: Sciaridae), adults of different light intensities. HortScience. 42, 1217–1220
Degen T, Mitesser O, Perkin EK, Weiß NS, Oehlert M, Mattig E, Hölker F (2016). Street lighting: sex-independent impacts on moth movement. Journal of Animal Ecology. 85, 1352–1360.
Dobzhansky T (1924). Die geographische und individuelle Variabilitat von Harmonia axyridis Pall in ihren Wechselbeziehungen. Biologisches Zentralblatt. 44, 401–421.
Dobzhansky T (1933). Geographical variation in lady-beetles. American Naturalist, 67: 97–126.
Eisenbeis G, Eick K (2010) Attraction of nocturnal insects to street lights with special regard to LEDs. In: Abstracts of the Society for Conservation Biology, 24th Annual Meeting, Edmonton, Alberta
Eisenbeis G, Hassel F (2000) Zur Anziehung nachtaktiver Insekten durch Straßenlaternen—eine Studie kommunaler Beleuchtung-seinrichtungen in der Agrarlandschaft Rheinhessens. Natur und Landschaft 75(4), 145–156
Frank KD (1988). Impact of outdoor lighting on moths: An assessment. Journal of the Lepidopterists’ Society 42, 63–93.
Frolich MW (1976). Appearance of vegetation in ultraviolet light: absorbing flowers, reflecting backgrounds. Science 194, 839–841.
Garris HW, Snyder JA (2010). Sex-specific Attraction of Moth Species to Ultraviolet Light Traps. Southeastern Naturalist. 9(3), 427–434
Goldsmith TH (1961). The color vision of insects. Pages 771–794 in W. D. McElroy and B. Glass, editors. Light and life. Johns Hopkins Press, Baltimore, Maryland, USA.
Gorostiza EA, Colomb J, Brembs B (2016). A decision underlies phototaxis in an insect. Open Biology. 6: 160229. http://dx.doi.org/10.1098/rsob.160229.
Graig CL, Bernard GD (1990). Insect attraction to ultraviolet-reflecting spider webs and web decorations. Ecology, 71(2), 616–623
Gregg PC, Fitt GP, Coombs M, Henderson GS (1994). Migrating moths collected in tower-mounted light traps in northern New South Wales, Australia: Influence of local and synoptic weather. Bulletin of Entomological Research 84,17–30.
Hesler LS, Kieckhefer RW, Catangui MA (2004). Surveys and field observations of Harmonia axyridis and other Cocci-nellidae (Coleoptera) in Eastern and Central South Dakota. Transactions of the American Entomological Society. 130, 113–133.
Hodek I, Honěk A (1996). Ecology of Coccinellidae. Kluwer Academic Publishers. Dordrecht. 464 pp.
Hu GG, Stark WS (1977). Specific receptor input into spectral preference in Drosophila. Journal of Comparative Physiology. 121, 241–252.
Kelber A, Vorobyev M, Osorio D (2003). Animal colour vision - behavioural tests and physiological concepts. Biological Reviews, 78(1), 81–118.
Koch R.L, Hutchison WD (2003). Phenology and Blacklight Trapping of the Multicolored Asian Lady Beetle (Coleoptera: Coccinellidae) in a Minnesota Agricultural landscape. Journal of Entomological Science. 38(3), 477–480
Komai T (1956), Genetics of ladybeetles. Advance Genetics. 8, 155–188.
LaMana ML, Miller JC (1996). Field observations on Harmonia axyridis Pallas (Coleoptera: Coccinellidae) in Oregon. Biological Control 6, 232–237.
Land MF (1997). Visual acuity in insects. Annual Review of Entomology. 42, 147–177.
Levine E (1989). Forecasting Hydraecia immanis (Lepidoptera: Noctuidae) moth phenology based on light-trap catches and degree-day accumulations. Journal of Economic Entomology. 82,433–438.
McCornack BP, Koch RL, Ragsdale DW (2007). A simple method for in-field sex determination of the multicolored Asian lady beetle Harmonia axyridis. Journal of insect science. 7(10): 1–12
McEwen RS (1918). The reactions to light and to gravity in Drosophila and its mutants. Journal of Experimental Zoology. 25, 49–106.
Meinertzhagen IA, Menzel R, Kahle G (1983). The identification of spectral receptor types in the retina and lamina of the dragonfly Sympetrum rubicundulum. Journal of Comparative Physiology A. 151, 295–310.
Michie LJ, Mallard F, Majerus MEN, Jiggins FM (2010). Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis.Journal of Evolutionary biology. 23, 1699–1707
Mikkola K (1972). Behavioural and electrophysiological responses of night-flying insects, especially Lepidoptera, to near‐ultraviolet and visible light. Annales Zoologici Fennici. 9, 225–254.
Nabli H, Bailey WC, Necibi S (1999). Beneficial insect attraction to light traps with different wavelengths. Biological Control. 16, 185–188.
Nalepa CA (2013). Coccinellidae captured in blacklight traps: Seasonal and diel pattern of the dominant species Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology. 110, 593–597
Nalepa CA, Kidd KA, Ahlstrom KR (1996). Biology of Harmonia axyridis (Coleoptera: Coccinellidae) in winter aggregations. Annals of the Entomological Society America. 89, 681–685.
Nedved O, Kalushkov P (2012). Effect of air humidity on sex ratio and development of ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Psyche, 2012, 173482
Osawa N (2001). The effect of hibernation on the seasonal variations in adult body size and sex ratio of the polymorphic ladybird beetle Harmonia axyridis: the role of thermal melanism. Acta Societatis Zoologicae Bohemicae 65, 269–278
Osawa N, Nishida T (1992). Seasonal variation in elytral color polymorphism in Harmonia axyridis (the ladybird beetle) – the role of nonrandom mating. Heredity 69, 297–307.
Owens ACS, Lewis SM (2018). The impact of artificial light at night on nocturnal insects: A review and synthesis. Ecology and Evolution. 8, 11337–11358.
Ramamurthy VV, Akhtar MS, Patankar N, Menon P, Kumar R, Singh SK et al. (2010) Efficiency of different light sources in light traps in monitoring insect diversity. Munis Entomology & Zoology. 5(1), 109–114.
Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, Martin GS, Martinkova Z, Minnaar IA, Nedved O, Orlova-Bienkowskaja MJ, Osawa N, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, Wielink P, Viglásová S, Zach P, Zakharov IA, Zaviezo T, Zhao Z (2016). The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biological Invasions. 18, 997–1044
Schwind R (1985). Sehen unter und iber Wasser, Sehen von Wasser. Naturwissenschaften 72, 343–352.
Seo MJ, Kim GH, Youn YN (2008). Differences in biological and behavioural characteristics of Harmonia axyridis (Coleoptera: Coccinellidae) according to colour patterns of elytra. Journal of Applied Entomology. 132, 239–247.
Silberglied RE (1979). Communication in the ultraviolet. Annual Review of Ecology and Systematics 10, 373–398.
Soares AO, Coderre D, Schanderl H (2001). Fitness of two phenotypes of Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology 98, 287–293.
Somers-Yeates R, Hodgson D, McGregor PK, Spalding A, Ffrench-Constant RH (2013). Shedding light on moths: Shorter wavelengths attract noctuids more than geometrids. Biology Letters. 9, 20130376.
Southwood TRE (1978). Ecological Methods with Particular Reference to the Study of Insect Populations. 2nd ed. Chapman and Hall, London, 524 pp.
Southwood TRE, Henderson PA (2000). Ecological methods. Blackwell Science, UK. p 269–292.
Tedders WL, Schaefer PW (1994) Release and establish-ment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomol. News 105, 228–243
Thomas AW, GM Thomas (1994). Sampling strategies for estimating moth species diversity using a light trap in a northeastern softwood forest. Journal of the Lepidopterists’ Society 48, 85–105.
Thomas CD (1989). Limits and scope of light-trapping for studying moth population dynamics. New Zealand Entomologist 12, 89–90.
van Grunsven RHA, Donners M, Boekee K, Tichelaar I, van Geffen KG, Groenendijk D. Veenendaal, E. M. (2014). Spectral composition of light sources and insect phototaxis, with an evaluation of existing spectral response models. Journal of Insect Conservation, 18, 225–231.
van Langevelde F, Ettema JA, Donners M, WallisDeVries MF, Groenendijk D (2011). Effect of spectral composition of artificial light on the attraction of moths. Biological Conservation, 144, 2274–2281.
Wakefield A, Broyles M, Stone EL, Jones G, Harris S (2016). Experimentally comparing the attractiveness of domestic lights to insects: Do LEDs attract fewer insects than conventional light types? Ecology and Evolution. 00:1–9.
Worth CB, Muller J (1979). Captures of large moths by an ultraviolet light trap. Journal of the Lepidopterists’ Society. 33, 261–264.
Yathom S (1981). Sex ratio and mating status of Earias insulana females (Lepidoptera: Noctuidae) collected from light traps in Israel. Israel Journal of Entomology 15, 97–100.

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Comparative function of blacklight and visual light sources in capturing Harmonia axyridis in the field and laboratory conditions; effect of color polymorphism

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Abstract

Figures

Introduction

Materials And Methods

1. Light Traps

2. Foliage Beating

Laboratory Studies

2.1 Two-choice experiment

2.2 Non-choice Experiment

Results

Light trap and foliage sampling

Sex Ratio

Indoor Experiments

Discussion

Declarations

References

Additional Declarations

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