Long-Lasting Bisexual Lures for Assessing Moth Biodiversity and Monitoring Alien Species in Zoos and Botanical Gardens: Case Study in Zoo of Debrecen (NE Hungary)
by
, ,
Szabolcs Szanyi
1,*
,
Csenge Lelle Kovács
1,
Miklós Tóth
2,
Ottó Lincz
3,
Gergely Sándor Nagy
3,
Zoltán Varga
4 and
Antal Nagy
1 1
Faculty of the Agricultural and Food Sciences and Environmental Management, Institute of Plant Protection, Debrecen, University of Debrecen, Böszörményi út 138., H-4032 Debrecen, Hungary
2
Plant Protection Institute, CAR, HUN-REN, H-1525 Budapest, Hungary
3
Zoo Debrecen, Ady Endre Str. 1–3, H-4032 Debrecen, Hungary
4
Department of Evolutionary Zoology and Human Biology, University of Debrecen, Egyetem tér 1, H-4010 Debrecen, Hungary
*
Author to whom correspondence should be addressed.
J. Zool. Bot. Gard. 2025, 6(1), 11; https://doi.org/10.3390/jzbg6010011
Submission received: 23 November 2024
/
Revised: 19 January 2025
/
Accepted: 3 February 2025
/
Published: 7 February 2025
(This article belongs to the Special Issue Invasive Species in Botanical and Zoological Gardens)
Abstract
Zoos and botanical gardens have a special role in the promotion, presentation and conservation of biodiversity in urbanised environments. Additionally, they provide special habitats for alien and invasive species. The formerly used methods of biodiversity assessments (e.g., light trapping, transect counts, etc.) are mostly labour-intensive and/or not efficient enough. In the Zoo of Debrecen, the efficacy and suitability of a synthetic (FLO) and a semisynthetic (SBL) lure for this purpose were proven. The qualitative and quantitative compositions of a moderately rich moth assemblage including 52 moth species were revealed, and the appearance and population dynamics of three invasive (Helicoverpa armigera, Autographa gamma and Cydalima pespectalis) and nine harmful pest species were also recorded. The results proved that the lures tested and traps used provide an easy-to-use, standardised and relatively cheap method for Zoos and botanical gardens to assess their biodiversity even in the case of limited resources.
1. Introduction
Urban and suburban parks often sustain a surprisingly high moth diversity in densely populated regions [1,2,3]. Debrecen is the second largest town in Hungary with more than 200,000 inhabitants. The Zoo at the northern suburban area of the city acts as a multifunctional garden, serving the well-being and education of the local and regional society, visited by several tens of thousands of people per year. The park preserves a part of the Nagyerdő (Debrecen’s Great Forest), which is one of the last remains of a native oak forest formerly covering significant parts of the region. However, the area suffers from pressure from communal traffic, the light pollution of the neighbouring urban areas, the sinking of the ground water table, intensive forestry and park management (mowing, fertilising, planting alien species, etc.) and other anthropogenic disturbances.
Therefore, we conducted a survey of night-active moths to identify, on one hand, which components of the nature-like moth assemblages of the region have been preserved and, on the other, what economically important species (incl. pests, aliens and invasives) have colonised in this semi-natural but disturbed suburban habitat. At the same time, we tested recently developed methods using feeding attractant semiochemicals that can complement and, in some cases, even substitute the widely used light and pheromone traps [4]. The attraction of noctuid moths to phenylacetaldehyde was reported on decades ago [5], and in North American experiments, the attractivity of isoamyl alcohol was also proven [6,7]. However, these semiochemicals were not efficient enough for practical use in insect trapping. In Hungary, experiments were started in the late 1990s by the CSALOMON® research group of the Plant Protection Institute of CAR, HUN-REN (Budapest, Hungary). As a result, a new series of innovative feeding attractants including combinations of the mentioned compounds and synthetic and/or organic (e.g., red wine) synergist materials was developed [8]. One of the most efficient type of lures is the synthetic, floral scent-like FLO (floral) lure containing phenylacetaldehyde, (E)-anethol, benzyl acetate and eugenol (1:1:1:1). Another semisynthetic lure with the scent of fermenting liquids is the SBL (semisynthetic bisexual lure) which contains isoamyl alcohol, acetic acid and red wine (1:1:1). Further details on these lures and a discussion on their efficiency and selectivity can be found in [4,9,10].
Based on experiments performed mainly in the Carpathian Lowland (Hungary, West Romania and West Ukraine), traps baited with these feeding attractants proved to be easy-to-use, standardised and efficient tools for studying moth assemblages in nature-like, semi-natural and anthropogenic ecosystems. This method provided new results for both basic studies (faunistical, biogeographical and ecological) and practical applications (pest management, forestry and nature conservation) [9,10,11,12,13,14,15]. Beyond the faunistical and ecological surveys, traps were used for detecting and monitoring several invasive pests e.g., the Cotton Bollworm (Helicoverpa armigera Hb.) [16]. Traps with such or similar lures were used on the Beet Armyworm (Spodoptera exigua Hb.) [17] and the East Asian Buxus moth (Cydalimna perspectalis Wlk.) [18,19]. Botanical and Zoological Gardens often provide suitable habitats for such alien species (pests and invasives); however, they are traditionally overlooked or under-studied. Our study provides data on the role of these non-traditionally managed areas both in terms of biodiversity conservation and how they serve as a potential refuge, source and/or “stepping stone” for alien and invasive species. Additionally, a new, easy-to-use, standardised innovative method for studying them is also promoted.
2. Materials and Methods
2.1. Field Tests
Trappings were carried out at the Zoo of Debrecen in Hungary. Traps were hung on trees, at a height of 1.8–2 m at a 20–25 m distance from each other, at the border of the park, in a margin of a deciduous forest. The test was run 25 May–5 October 2023. Both types of baited traps were used in eight repetitions (8 × 2 = 16 traps in total). Lures were replaced monthly with new ones. Traps were checked, and samples (individuals caught) were taken weekly.
2.2. Traps
CSALOMON® VARL+ funnel traps were used (Plant Protection Institute, CAR, HUN-REN, Budapest; photos of the trap can be viewed at www.csalomontraps.com (accessd on 20 October 2024)). Similar traps have routinely been used for trapping several noctuids [4,8,11]. To kill captured insects, a small piece (1 × 1 cm) of a household anti-moth insecticide strip (Chemotox® SaraLee, Temana Intl. Ltd., Slouth, UK; active ingredient 15% dichlorvos) was placed into the container of traps.
2.3. Baits
SBL: 1:1:1 mixture of isoamyl alcohol, acetic acid and red wine, filled in 4 mL polypropylene tubes. The mixture was administered to dental rolls inside the tubes and could evaporate through a small opening (Ø = 4 mm), which was opened at the time the mixture was set out [9,10,13,14].
FLO lure: mixture of phenylacetaldehyde, (E)-anethol, benzyl acetate and eugenol (1:1:1:1). The compounds evaporated through the wall of the polyethylene bag dispensers used [20].
2.4. Data Analysis
The insects caught by traps were identified at the species level, and their abundance was provided for each sample. Lepidoptera taxa were identified according to Varga [21]; the taxonomic list follows the system of Lafontaine and Schmidt [22], with the modifications of Zahiri et al. [23]. The number, relative frequency and ratio of the families, subfamilies and species were provided for the whole sample and for the two lure types tested separately. The number and ratio of pests, invasive species, differential species (species caught only with a given lure type) and the species belonging to different life forms were also given. The pest status was determined based on Mészáros and Szabóky [24,25] and Zúbrik et al. [26], and in the case of life forms, Varga et al. [27] was followed.
These values were used to present the formerly described selectivity and attractivity of baits and proved the ability of traps to be used to assess the biodiversity and monitoring of several alien species in the special kind of habitat studied.
3. Results
During the 133-day sampling period, 52 moth species (Table 1) were caught, with 1943 individuals of which 31.6% were females. Regarding the number of species caught, the SBL was more effective since it attracted 43 species, while the FLO traps caught 19 species. Nevertheless, considering the abundances, SBL traps were less effective since they caught a lot fewer individuals (566) than the FLO traps (1377). The species caught belonged to six families, of which Noctuidae was the most species-rich and abundant, followed by Erebidae, Crambidae, Geometridae, Pyralidae and Thyatiridae (Figure 1).
The number of differential species of SBL traps was higher, especially regarding the most abundant families of Noctuidae and Erebidae, while the two species belonging to the Thyatiridae family were caught only by this lure type. On the other hand, in the case of Geometridae, only FLO traps had two different species. Except these specificities, the lures tested attracted species of most families similarly; nevertheless, both the qualitative and quantitative compositions of the samples taken with different lure types showed notable differences (Figure 1).
The relative frequencies of only six species were higher than 5%. Four of them belonged to Noctuidae (Amphipyra pyramidea L.: 5.9%; Abrostola triplasia L.: 9.4%; Autographa gamma L.: 5.8% and Dypterygia scabriuscula L.: 6.0%), while one belonged to the Erebidae (Amata phegea L.: 26.0%) and another to the Crambidae (Patania ruralis Scop.: 21.1%) family. Four of these most abundant species (P. ruralis, A. phagea, A triplasia and A. gamma) were caught almost only by FLO traps, while D. scabriuscula was a differential species for the SBL. The subdominant Macdunnoughia confusa Step. (4.7%) was attracted by the FLO lure, while Noctua pronuba L. (4.2%) and Trachea atriplicis L. (4.2%) preferred the SBL.
Due to the relatively low number of moths captured, only the phenology of the most abundant species could be characterised. A. phegea was monovoltine with a swarming period of about four weeks with a peak at mid-June. A. triplasia, A. gamma and M. confusa were on the wing from early June to mid-October, with an unexpected third peak between mid-September and October, probably referring to a formerly not recorded third generation. The adults of D. scabriuscula, T. atriplicis and A. pyramidea showed a long swarm from early June to August, without any high peaks, while P. ruralis had a similar long flying period with a late unusual peak in September, referring to a second or third generation in the given year. Some probably migrating individuals of the worldwide important pest Helicoverpa armigera were caught at the end of the vegetation period until mid-October.
The lures tested showed different attractivity to species belonging to different life forms referring to the habitat and food source preferences of species [27,28]. Generalist species mostly belonging to the Noctuidae family were mainly attracted by the SBL, and the Silvicolous species showed a similar preference (Table 2). In contrast, the species of the migratory and Altoherbosa (tall forb) life forms exclusively preferred the FLO lure. This seems to be the consequence of the taxonomic composition, since one of them (migratory species) belongs to the Heliothinae subfamily; however, the other six (four Altoherbosa and two migratory species), feeding on tall forbs and preferring Urtica dioica, all belong to the Plusiinae subfamily. Beyond that, most of the individuals of the only Lichenophagous species A. phegea were caught also with FLO traps (Table 2).
In the studied habitat, our traps caught three invasive and nine pest species. In total, they gave 23.1% of the species, and their relative frequency was 18.9% in total (Figure 2). Among them, Cydalima perspectalis was introduced from East Asia to Europe and spread through the continent in the last decade [18]. The widely distributed harmful pest species H. armigera was a subdominant, while the migratory A. gamma was an abundant member of the local assemblage. The latter has a more or less stabile native population in the Carpathian Basin but also belongs to the migratory species in other regions. Other pests had only low abundances, but their appearance referred to the disturbances and special character of the studied habitat (Figure 2, Table 2).
4. Discussion
Intensive urbanisation has destroyed not only lots of natural and semi-natural habitats but also fragmented and isolated their remaining patches in city parks, gardens, etc. [2,29,30]. Since urbanisation is seeming to accelerate [31,32], a further decline, isolation and extinction of local populations may be expected, including that of plants and animals, birds and moths, etc. [1,33,34]. Thus, surveying and understanding the effects of urbanisation on populations and communities constitute high-priority tasks that need innovative methods and solutions.
While recent surveys on night-active insects mostly used traditional methods such as light trapping with actinic tubes or mercury vapor lamps e.g., [1,2,3], in the present study, two recently developed [4,8,11] bisexual lures, SBL and FLO, were used. These lures proved to be attractive and selective mainly for species belonging to the Noctuidae, Erebidae and Crambidae families. Considering the number of species caught, the SBL was more efficient and was selective to Xyleninae and Noctuinae species, while the less effective FLO provided more data on Plusiinae species. Because of the different selectivity, these lures complement each other, and their parallel use can be recommended for biodiversity assessment, as was formerly published [4]. The general composition of the samples was quite similar to the samples of light traps, showing some unique characters [4,10,15]. The method used provided reliable data on the moth assemblages of the suburban park of Debrecen Zoo, with the high dominance of Noctuidae, Erebidae and Crambidae; in this respect, the results were similar to those obtained with samples in different suburban areas of Delhi, India [3], with other methods.
Despite the complexity of habitats, including small fragments of natural woody vegetation, the number of species recorded was relatively low, compared to the species richness of neighbouring forests in the NE Hungarian lowland [10,12]. The nearly complete absence of oakwood components is especially remarkable (Table 2). The number and abundances of economically important species were also low. Nevertheless, the appearance of the migrating Autographa gamma and Helicoverpa armigera and relatively large numbers of generalists such as Noctua pronuba, Amphipyra pyramidea, Dypterigia scabriuscula and Trachea atriplicis were also recorded.
The lures tested proved to be appropriate for assessing diversity and describing the composition of a moth assemblage, and they provide an easy-to-use, standardised and cost- and labour-effective method. The efficiency and simplicity of this method make it suitable for both large-scale and long-term experiments, collecting comparable data on insect communities including different taxa (e.g., Lepidoptera, Bombus sp., Diptera, Orthoptera, etc.) [35,36,37]. In conclusion, the presentation, promotion and also the conservation of biodiversity are all important missions of zooparks and botanical gardens, which need these kinds of innovative solutions, especially considering the usually limited resources available for environmental monitoring.
Author Contributions
Conceptualisation, S.S. and A.N.; Methodology, S.S., M.T., O.L., G.S.N. and A.N.; Investigation, S.S., C.L.K. and O.L.; Writing—original draft preparation, S.S., Z.V. and A.N.; Writing—review and editing, all authors. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by National Research Development and Innovation Office, grant number PD 138329.
Data Availability Statement
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Conflicts of Interest
The authors declare no conflicts of interest.
References
- Lintott, P.R.; Bunnefeld, N.; Fuentes-Montemayor, E.; Minderman, J.; Blackmore, L.M.; Goulson, D.; Park, K.J. Moth species richness, abundance and diversity in fragmented urban woodlands: Implications for conservation and management strategies. Biodivers. Conserv. 2014, 23, 2875–2901. [Google Scholar] [CrossRef]
- Ellis, E.E.; Wilkinson, T.L. Moth assemblages within urban domestic gardens respond positively to habitat complexity, but only at a scale that extends beyond the garden boundary. Urban Ecosyst. 2020, 24, 469–479. [Google Scholar] [CrossRef]
- Paul, M. Impact of urbanization on moth (Insecta: Lepidoptera: Heterocera) diversity across different urban landscapes of Delhi, India. Acta Ecol. Sin. 2021, 41, 204–209. [Google Scholar] [CrossRef]
- Szanyi, S.; Molnár, A.; Szanyi, K.; Tóth, M.; Jósvai, J.; Varga, Z.; Nagy, A. Traps with synthetic, bisexual generic attractants as a new method supplementing light traps for assessing composition and diversity of Macroheterocera assemblages. Sci. Rep. 2024, 14, 20212. [Google Scholar] [CrossRef]
- Cantelo, W.W.; Jacobson, M. Phenylacetaldehyde attracts moths to bladder flower and to blacklight traps. Environ. Entomol. 1979, 8, 444–447. [Google Scholar] [CrossRef]
- Landolt, P.J. New chemical attractants for trapping Lacanobia subjuncta, Mamestra configurata, and Xestia c-nigrum (Lepidoptera: Noctuidae). J. Econ. Entomol. 2000, 93, 101–106. [Google Scholar] [CrossRef]
- Landolt, P.J.; Alfaro, J.F. Trapping Lacanobia subjuncta, Xestia c-nigrum and Mamestra configurata (Lepidoptera: Noctuidae) with acetic acid and 3-methyl-1-butanol in controlled relesase dispensers. Environ. Entomol. 2001, 30, 656–662. [Google Scholar] [CrossRef]
- Tóth, M.; Szarukán, I.; Dorogi, B.; Gulyás, A.; Nagy, P.; Rozgonyi, Z. Male and female noctuid moths attracted to synthetic lures in Europe. J. Chem. Ecol. 2010, 36, 592–598. [Google Scholar] [CrossRef]
- Nagy, A.; Szarukán, I.; Gém, F.; Nyitrai, R.; Füsti-Molnár, B.; Némerth, A.; Kozák, L.; Molnár, A.; Katona, K.; Szanyi, S.; et al. Preliminary data on the effect of semi-synthetic baits for Noctuidae (Lepidoptera) on the non-target Lepidoptera species. Acta Agrar. Debreceniensis 2015, 66, 71–80. [Google Scholar] [CrossRef]
- Szanyi, S.; Nagy, A.; Molnár, A.; Katona, K.; Tóth, M.; Varga, Z. Night-active Macroheterocera species in traps with synthetic attractants in the Velyka Dobron’ Game Reserve (Ukraine, Transcarpathia). Acta Zool. Acad. Sci. Hung. 2017, 63, 97–114. [Google Scholar] [CrossRef]
- Tóth, M.; Szarukán, I.; Nagy, A.; Gém, F.; Nyitrai, R.; Kecskés, Z.; Krakkó, L.; Jósvai, J.K.; Bélai, I. Félszintetikus “biszex” csalétkek kártevő rovarok nőstényeinek és hímjeinek fogására [Semi-synthetic “bisex” baits for catching of males and females of pest species]. Növényvédelem 2015, 51, 197–205. [Google Scholar]
- Szanyi, S.; Molnár, A.; Kozák, L.; Szalárdi, T.; Varga, Z.; Tóth, M.; Nagy, A. Nyírségi Macroheterocera együttesek vizsgálata illatanyagcsapdák alkalmazásával—[Study on the Macroheterocera assemblages of the Nyírség (Northeast Hungary) using volatile traps—In Hungarian]. Erdészettudományi Közlemények 2019, 9, 51–68. [Google Scholar] [CrossRef]
- Szanyi, S.; Szarukán, I.; Nagy, A.; Jósvai, J.; Imrei, Z.; Varga, Z.; Tóth, M. Comparing performance of synthetic sex attractants and a semisynthetic bisexual lure in Orthosia and Conistra species (Lepidoptera: Noctuidae). Acta Phytopathol. Entomol. Hung. 2020, 55, 115–122. [Google Scholar] [CrossRef]
- Szanyi, S.; Varga, Z.; Nagy, A.; Jósvai, J.K.; Imrei, Z.; Tóth, M. Bisexual lures and their comparison with synthetic sex attractants for trapping Orthosia species (Lepidoptera: Noctuidae). J. Appl. Entomol. 2022, 146, 1109–1115. [Google Scholar] [CrossRef]
- Szalárdi, T.; Szanyi, S.; Szarukán, I.; Tóth, M.; Nagy, A. Semiochemical baited traps of lepidopteran pests of economic importance can deliver reliable data also on wide range of non-target species: Case study in the Hajdúság Region of East Pannonian Lowland (East Hungary). Biodivers. Data J. 2021, 9, e72305. [Google Scholar] [CrossRef] [PubMed]
- Tóth, M.; Nagy, A.; Szarukán, I.; Ary, K.; Cserenyec, A.; Fenyődi, B.; Gombás, D.; Lajkó, T.; Merva, L.; Szabó, J.; et al. One Decade’s Research Efforts in Hungary to Develop a Bisexual Lure for the Cotton Bollworm Helicoverpa armigera Hübner. Acta Phytopathol. Entomol. Hung. 2020, 55, 53–62. [Google Scholar] [CrossRef]
- Chowdary, L.R.; Kumar, G.V.S.; Bharathi, S.; Sarada, O.; Nagaraju, Y.; Chandrashekara, K.M.; Harish, G.N. Off-season survival and life history of beet armyworm, Spodoptera exigua (Hubner) on various host plants. Sci. Rep. 2024, 14, 13721. [Google Scholar] [CrossRef]
- Molnár, B.P.; Kárpáti, Z.; Nagy, A.; Szarukán, I.; Csabai, J.; Koczor, S.; Tóth, M. Development of a Female-Targeted Lure for the Box Tree Moth Cydalima perspectalis (Lepidoptera: Crambidae): A Preliminary Report. J. Chem. Ecol. 2019, 45, 657–666. [Google Scholar] [CrossRef]
- Nagy, A.; Szarukán, I.; Csabai, J.; Molnár, A.; Molnár, B.P.; Kárpáti, Z.; Szanyi, S.; Tóth, M. Distribution of the box tree moth (Cydalima perspectalis Walker 1859) in the north-eastern part of the Carpathian Basin with a new Ukrainian record and Hungarian data. EPPO Bull. 2017, 47, 279–282. [Google Scholar] [CrossRef]
- Tóth, M.; Répási, V.; Szocs, G. Chemical attractants for females of pest Pyralids and Phycitids (Lepidoptera: Pyralidae, Phycitidae). Acta Phytopathol. Entomol. Hung. 2002, 37, 375–384. [Google Scholar] [CrossRef]
- Varga, Z. Magyarország Nagylepkéi—Macrolepidoptera of Hungary; Heterocera Press: Budapest, Hungary, 2012; p. 354. [Google Scholar]
- Lafontaine, D.; Schmidt, C. Annotated check list of the Noctuoidea (Insecta, Lepidoptera) of North America north of Mexico. ZooKeys 2010, 40, 1–239. [Google Scholar] [CrossRef]
- Zahiri, R.; Holloway, J.D.; Kitching, I.J.; Lafontaine, J.D.; Mutanen, M.; Wahlberg, N. Molecular phylogenetics of Erebidae (Lepidoptera, Noctuoidea). Syst. Entomol. 2011, 37, 102–124. [Google Scholar] [CrossRef]
- Mészáros, Z.; Szabóky, C. A Magyarországi Molylepkék Gyakorlati Albuma; Balázs, K., Ed.; Agroinform: Budapest, Hungary, 2005; pp. 1–178. [Google Scholar]
- Mészáros, Z.; Szabóky, C. A Magyarországi Nagylepkék Gyakorlati Albuma; Szalkay József Magyar Lepkészeti Egyesület: Budapest, Hungary, 2012; p. 185. [Google Scholar]
- Zúbrik, M.; Kunca, A.; Csóka, G. Insects and Diseases Damaging Trees and Shrubs of Europe; Zúbrik, M., Kunca, A., Csóka, G.N.A.P., Eds.; NAP: Ann Arbor, MI, USA, 2013; 535p, Available online: www.napeditions.com (accessed on 12 November 2024).
- Varga, Z.; Ronkay, L.; Bálint, Z.; László, M.G.; Peregovits, L. Checklist of the Fauna of Hungary; Macrolepidoptera; Hungarian Natural History Museum: Budapest, Hungary, 2004; Volume 3, p. 106. [Google Scholar]
- Varga, Z. Zoogeographic division of Hungary based on components of the Macrolepidoptera-fauna (in Hung. with German summary). Folia Entomol. Hung. 1964, 17, 119–167. [Google Scholar]
- McKinney, M.L. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 2006, 127, 247–260. [Google Scholar] [CrossRef]
- Di Mauro, D.; Dietz, T.; Rockwood, L. Determining the effect of urbanization on generalist butterfly species diversity in butterfly gardens. Urban Ecosyst. 2007, 10, 427–439. [Google Scholar] [CrossRef]
- Seto, K.C.; Güneralp, B.; Hutyra, L.R. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc. Natl. Acad. Sci. USA 2012, 109, 16083–16088. [Google Scholar] [CrossRef]
- Aronson, M.F.J.; La Sorte, F.A.; Nilon, C.H.; Katti, M.; Goddard, M.A.; Lepczyk, C.A.; Warren, P.S.; Williams, N.S.G.; Cilliers, S.; Clarkson, B.; et al. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc. R. Soc. B Biol. Sci. 2014, 281, 20133330. [Google Scholar] [CrossRef]
- Rickman, J.K.; Connor, E.F. The effect of urbanization on the quality of remnant habitats for leaf-mining Lepidoptera on Quercus agrifolia. Ecography 2003, 26, 777–787. [Google Scholar] [CrossRef]
- Merckx, T.; Marini, L.; Feber, R.E.; Macdonald, D.W. Hedgerow trees and extended-width field margins enhance macro-moth diversity: Implications for management. J. Appl. Ecol. 2012, 49, 1396–1404. [Google Scholar] [CrossRef]
- Arnóczkyné Jakab, D.A.; Tóth, M.; Szarukán, I.; Szanyi, S.; Józan, Z.; Sárospataki, M.; Nagy, A. Long-term changes in the composition and distribution of the Hungarian bumble bee fauna (Hymenoptera, Apidae, Bombus). J. Hymenopt. Res. 2023, 96, 207–237. [Google Scholar] [CrossRef]
- Nagy, A.; Katona, P.; Molnár, A.; Rádai, Z.; Tóth, M.; Szanyi, K.; Szanyi, S. Wide range of brachyceran fly taxa attracted to synthetic and Semi-Synthetic generic noctuid lures and the description of new attractants for sciomyzidae and heleomyzidae families. Insects 2023, 14, 705. [Google Scholar] [CrossRef]
- Nagy, A.; Ősz, A.; Tóth, M.; Rácz, I.A.; Kovács, S.; Szanyi, S. Nontarget catches of traps with chemical lures may refer to the flower-visitation, probable pollination, and feeding of bush crickets (Ensifera: Tettigoniidae). Ecol. Evol. 2023, 13, e10249. [Google Scholar] [CrossRef] [PubMed]
Figure 1.
Composition of whole Lepidoptera sample and samples collected with different lure types (SBL and FLO) regarding number of species and individuals caught by families.
Figure 1.
Composition of whole Lepidoptera sample and samples collected with different lure types (SBL and FLO) regarding number of species and individuals caught by families.
Figure 2.
Ratio and relative frequencies of invasive and pest species in moth assemblage of Zoo of Debrecen.
Figure 2.
Ratio and relative frequencies of invasive and pest species in moth assemblage of Zoo of Debrecen.
Table 1.
A list of the moths caught at the Zoo of Debrecen in 2023 with traps baited with phenylacetaldehyde-based (FLO) and isoamyl alcohol-based (SBL) lures.
Table 1.
A list of the moths caught at the Zoo of Debrecen in 2023 with traps baited with phenylacetaldehyde-based (FLO) and isoamyl alcohol-based (SBL) lures.
| Family | Subfamily | Species | FLO | SBL |
|---|---|---|---|---|
| Crambidae | Spilomelinae | Cydalima perspectalis (Walker, 1859) | + | + |
| Crambidae | Patania ruralis (Scopoli, 1763) | + | + | |
| Pyralidae | Phycitinae | Plodia interpunctella (Hübner, [1813]) | + | + |
| Thyatiridae | Thyatirinae | Habrosyne pyritoides (Hufnagel, 1766) | + | |
| Thyatiridae | Thyatirinae | Tethea or ([Denis & Schiffermüller], 1775) | + | |
| Geometridae | Ennominae | Ligdia adustata ([Denis & Schiffermüller], 1775) | + | + |
| Geometridae | Sterrhinae | Idaea aversata (Linnaeus, 1758) | + | |
| Erebidae | Hypeninae | Hypena rostralis (Linnaeus, 1758) | + | |
| Erebidae | Scoliopteryginae | Scoliopteryx libatrix (Linnaeus, 1758) | + | |
| Erebidae | Catocalinae | Catocala promissa ([Denis & Schiffermüller], 1775) | + | + |
| Erebidae | Catocalinae | Catocala nupta (Linnaeus, 1767) | + | |
| Erebidae | Catocalinae | Lygephila pastinum (Treitschke, 1826) | + | |
| Erebidae | Ctenuchinae | Amata phegea (Linnaeus, 1758) | + | + |
| Erebidae | Ctenuchinae | Dysauxes ancilla (Linnaeus, 1767) | + | |
| Noctuidae | Acronictinae | Acronicta rumicis (Linnaeus, 1758) | + | |
| Noctuidae | Amphipyrinae | Amphipyra pyramidea (Linnaeus, 1758) | + | |
| Noctuidae | Plusiinae | Autographa gamma (Linnaeus, 1758) | + | |
| Noctuidae | Plusiinae | Trichoplusia ni (Hübner, [1803]) | + | |
| Noctuidae | Plusiinae | Macdunnoughia confusa Stephens, 1850 | + | + |
| Noctuidae | Plusiinae | Abrostola triplasia (Linnaeus, 1758) | + | + |
| Noctuidae | Plusiinae | Abrostola tripartita (Hufnagel, 1766) | + | |
| Noctuidae | Plusiinae | Diachrysia chrysitis (Linnaeus, 1758) | + | |
| Noctuidae | Plusiinae | Diachrysia stenochrysis (Warren, 1913) | + | |
| Noctuidae | Heliothinae | Helicoverpa armigera (Hübner, [1808]) | + | |
| Noctuidae | Hadeninae | Lacanobia oleracea (Linnaeus, 1758) | + | |
| Noctuidae | Hadeninae | Mamestra brassicae (Linnaeus, 1758) | + | |
| Noctuidae | Hadeninae | Hadena bicruris (Hufnagel, 1766) | + | |
| Noctuidae | Hadeninae | Mythimna turca (Linnaeus, 1761) | + | + |
| Noctuidae | Hadeninae | Mythimna vitellina (Hübner, [1808]) | + | |
| Noctuidae | Hadeninae | Mythimna albipuncta ([Denis & Schiffermüller], 1775) | + | + |
| Noctuidae | Noctuinae | Noctua pronuba (Linnaeus, 1758) | + | |
| Noctuidae | Noctuinae | Noctua fimbriata (Schreber, 1759) | + | |
| Noctuidae | Noctuinae | Noctua orbona (Hufnagel, 1766) | + | |
| Noctuidae | Noctuinae | Noctua janthe (Borkhausen, 1792) | + | |
| Noctuidae | Noctuinae | Agrotis segetum ([Denis & Schiffermüller], 1775) | + | |
| Noctuidae | Noctuinae | Agrotis exclamationis (Linnaeus, 1758) | + | |
| Noctuidae | Noctuinae | Agrotis bigramma (Esper, 1790) | + | |
| Noctuidae | Xyleninae | Charanyca trigrammica (Hufnagel, 1766) | + | |
| Noctuidae | Xyleninae | Dypterygia scabriuscula (Linnaeus, 1758) | + | |
| Noctuidae | Xyleninae | Trachea atriplicis (Linnaeus, 1758) | + | |
| Noctuidae | Xyleninae | Athetis gluteosa (Treitschke, 1835) | + | |
| Noctuidae | Xyleninae | Oligia latruncula ([Denis & Schiffermüller], 1775) | + | |
| Noctuidae | Xyleninae | Oligia strigilis (Linnaeus, 1758) | + | |
| Noctuidae | Xyleninae | Phlogophora meticulosa (Linnaeus, 1758) | + | |
| Noctuidae | Xyleninae | Cosmia affinis (Linnaeus, 1767) | + | |
| Noctuidae | Xyleninae | Thalpophila matura (Hufnagel, 1766) | + | |
| Noctuidae | Xyleninae | Apterogenum ypsillon ([Denis & Schiffermüller], 1775) | + | |
| Noctuidae | Xyleninae | Agrochola litura (Linnaeus, 1761) | + | |
| Noctuidae | Xyleninae | Tiliacea aurago ([Denis & Schiffermüller], 1775) | + | |
| Noctuidae | Xyleninae | Conistra vaccinii (Linnaeus, 1761) | + | |
| Noctuidae | Xyleninae | Conistra erythrocephala ([Denis & Schiffermüller], 1775) | + | |
| Noctuidae | Noctuinae | Xestia xanthographa ([Denis & Schiffermüller], 1775) | + |
Table 2.
The composition of the moth assemblage sampled considering the number (and ratio) and abundances (frequencies) of invasive and pest species and species belonging to different life forms of macro-moths.
Table 2.
The composition of the moth assemblage sampled considering the number (and ratio) and abundances (frequencies) of invasive and pest species and species belonging to different life forms of macro-moths.
| Species | Individuals | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| SBL | FLO | Sum | SBL | FLO | Sum | |||||||
| n | % | n | % | n | % | n | % | n | % | n | % | |
| Invasives | 1 | 2.3 | 3 | 15.8 | 3 | 5.8 | 1 | 0.2 | 155 | 11.3 | 156 | 8.0 |
| Pests | 2 | 4.7 | 9 | 47.4 | 9 | 17.3 | 88 | 15.5 | 144 | 10.5 | 232 | 11.9 |
| S | 43 | 19 | 52 | 566 | 1377 | 1943 | ||||||
| Life forms (macro-moths: 49 species, 1496 individuals) | ||||||||||||
| Generalist | 13 | 32.5 | 2 | 12.5 | 13 | 26.5 | 247 | 46.6 | 87 | 9.0 | 334 | 22.3 |
| Migratory | 0 | 0 | 3 | 18.75 | 3 | 6.1 | 0 | 0.0 | 150 | 15.5 | 150 | 10.0 |
| Steppic | 3 | 7.5 | 1 | 6.25 | 4 | 8.2 | 5 | 0.9 | 7 | 0.7 | 12 | 0.8 |
| Mesophilous | 3 | 7.5 | 2 | 12.5 | 4 | 8.2 | 7 | 1.3 | 14 | 1.4 | 21 | 1.4 |
| Altoherbosa | 1 | 2.5 | 4 | 25 | 4 | 8.2 | 9 | 1.7 | 200 | 20.7 | 209 | 14.0 |
| Moor–marsh | 2 | 5 | 0 | 0 | 2 | 4.1 | 2 | 0.4 | 0 | 0.0 | 2 | 0.1 |
| Silvicolous | 11 | 27.5 | 3 | 18.75 | 12 | 24.5 | 236 | 44.5 | 10 | 1.0 | 246 | 16.4 |
| Birch–alder | 1 | 2.5 | 0 | 0 | 1 | 2.0 | 1 | 0.2 | 0 | 0.0 | 1 | 0.1 |
| Oakwood | 1 | 2.5 | 0 | 0 | 1 | 2.0 | 3 | 0.6 | 0 | 0.0 | 3 | 0.2 |
| Willow–poplar | 4 | 10 | 0 | 0 | 4 | 8.2 | 13 | 2.5 | 0 | 0.0 | 13 | 0.9 |
| Lichenophagous | 1 | 2.5 | 1 | 6.25 | 1 | 2.0 | 7 | 1.3 | 498 | 51.6 | 505 | 33.8 |
| Sum | 40 | 16 | 49 | 530 | 966 | 1496 | ||||||
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Szanyi, S.; Kovács, C.L.; Tóth, M.; Lincz, O.; Nagy, G.S.; Varga, Z.; Nagy, A. Long-Lasting Bisexual Lures for Assessing Moth Biodiversity and Monitoring Alien Species in Zoos and Botanical Gardens: Case Study in Zoo of Debrecen (NE Hungary). J. Zool. Bot. Gard. 2025, 6, 11. https://doi.org/10.3390/jzbg6010011
AMA Style
Szanyi S, Kovács CL, Tóth M, Lincz O, Nagy GS, Varga Z, Nagy A. Long-Lasting Bisexual Lures for Assessing Moth Biodiversity and Monitoring Alien Species in Zoos and Botanical Gardens: Case Study in Zoo of Debrecen (NE Hungary). Journal of Zoological and Botanical Gardens. 2025; 6(1):11. https://doi.org/10.3390/jzbg6010011
Chicago/Turabian StyleSzanyi, Szabolcs, Csenge Lelle Kovács, Miklós Tóth, Ottó Lincz, Gergely Sándor Nagy, Zoltán Varga, and Antal Nagy. 2025. "Long-Lasting Bisexual Lures for Assessing Moth Biodiversity and Monitoring Alien Species in Zoos and Botanical Gardens: Case Study in Zoo of Debrecen (NE Hungary)" Journal of Zoological and Botanical Gardens 6, no. 1: 11. https://doi.org/10.3390/jzbg6010011
APA StyleSzanyi, S., Kovács, C. L., Tóth, M., Lincz, O., Nagy, G. S., Varga, Z., & Nagy, A. (2025). Long-Lasting Bisexual Lures for Assessing Moth Biodiversity and Monitoring Alien Species in Zoos and Botanical Gardens: Case Study in Zoo of Debrecen (NE Hungary). Journal of Zoological and Botanical Gardens, 6(1), 11. https://doi.org/10.3390/jzbg6010011
