Introduction

In the Azores archipelago the Laurel forests already dominated the landscape and could have occupied more than 2/3 of the territory. However, the Azorean islands were extremely impacted by human activities, mainly associated with a dramatic land-use changes (only about 5% of the original forests still remain; TRIANTIS et al., 2010), habitat degradation and the introduction of exotic and invasive species (CARDOSO et al., 2010; TRIANTIS et al., 2010; BORGES et al., 2013; TERZOPOULOU et al., 2015).

Currently, the Official Forestry Services rear Azorean endemic plant species, which seeks the restoration of the Laurel Forest and areas with high erosion risk or sensitive from the hydrological point of view, awareness-raising activities, and support forestation by private landowners (ROSAGRO et al., 2019). In São Miguel Island, most of these plants are reared in two forestry nurseries located in Povoação (Furnas) and Nordeste counties. Since 2008, nursery production of endemic woody plants has increased significantly, reaching in Furnas and the Nordeste, respectively, 55,000 and 80,000 plants annually (ROSAGRO et al., 2019). Among about 80 endemic plants that inhabit the Azorean archipelago (VIEIRA et al., 2020), eight species integrating the IUCN red list are reared in both forestry nurseries (Table 1).

The use of phytopharmaceutical products is limited to a single fungicide compound, which makes endemic plants vulnerable to attack by insect pests such as aphid and lepidopteran species (ROSAGRO et al., 2019). Preliminary studies allowed us to identify a major lepidopteran pest attacking Azorean endemic plants and one native species (Faia) (Table 1): Epiphyas postvittana (Walker, 1863) (Tortricidae), an exotic species commonly named the light brown apple moth (LBAM).

Epiphyas postvittana (Fig. 1) has a long list of synonyms (e.g., see VIVES MORENO, 2014; GBIF, 2021). It is native to Southeastern Australia, but has invaded Western Australia, New Zealand, Hawaii, New Caledonia, Australasia and Pacific Islands, Europe, United Kingdom, and California - USA (BROWN et al., 2010; SUCKLING & BROCKERHOFF, 2010; CABI, 2021). The species is recorded in numerous areas of biogeographic regions except for Antarctica (BROWN et al., 2010). In the Macaronesia region there are some records of the presence of LBAM, but in the Azores to date it was only cited on São Miguel, Pico, Terceira (VIEIRA & KARSHOLT, 2010; PÉREZ SANTA-RITA et al., 2018), and recently recorded to São Jorge and Flores islands (V. Vieira, unpublished). This species is considered introduced to the Macaronesia region, including in the Azores archipelago (VIEIRA & KARSHOLT, 2010).

In literature, LBAM is multivoltine and an economically important polyphagous pest species. The number of annual generations varies with latitude within its range. There is considerable overlap between generations, with development driven by temperature and larval host plant (BROWN et al., 2010; BUERGI, 2012; CABI, 2021). For example, in North America, E. postvittana completes 2-4 generations annually. Such in Australia (ZIELONKA et al., 2021), populations in California appear to undergo at least four generations and adults are active throughout the year. There is no winter resting stage, although overwintering larvae tend to develop slowly, with a lower threshold of development for all stages of 7.5ºC and an upper threshold of 31ºC (DANTHANARAYANA, 1975); 20ºC is the optimum for development, leading to a life cycle of 25 days (BUERGI, 2012). The variation in its cold response resulted in different forecasts of geographic distribution, which can have important management and regulatory implications (MOREY, 2015). The life cycle of adults lasts 2 to 3 weeks, depending on temperature and hostplant availability (BROWN et al., 2010).

Eggs are typically laid in clusters of 3-150 on the upper surface of leaves and take 8 days at 20ºC to hatch (THOMAS, 1975). These give rise to the first generation of larvae. The fully developed larvae are green and have a length from 10 to 20 mm (Fig. 1).

The larvae affect a wide range of horticultural and agricultural plant species in over 100 families (BROCKERHOFF et al., 2011; WANG et al., 2012). In the southeastern part of Australia and New Zealand, it is a pest on apples, grapes, berries, stone fruits, citrus, vegetable crops and numerous ornamentals (BROWN et al., 2010; WANG et al., 2012). In the Azores it occurs preferably in cultivated and garden areas (PÉREZ SANTA-RITA et al., 2018), and attacks the plants reared in forest nurseries. In the first stages, the larva feeds on the undersides of leaves within a silk chamber, later it continues to feed on leaves, leaf rollers, flowers, or perforate and enter the fruit, causing leaf twisting, browning, and drying out of the needles, inhibition of the stem growth, and leaf damages serve as foci for the establishment of some entomopathogenic microorganisms.

Global knowledge of natural enemies of LBAM is well reported (ADLER, 1991; WEARING et al., 1991; HOGG et al., 2013) and some spiders, chrysopids and mirids are cited as predators of larvae. Additionally, many hymenopteran parasitoids (braconids, ichneumonids and encyrtids) or tachinid flies attack the larval and egg stages.

The life cycle of LBAM and their natural enemies in the Azores archipelago are unknown. In this study we evaluated the temporal profile in the larval abundance of LBAM in eight endemic host plants grown in two forest nurseries on São Miguel Island. Besides some information on the abundance of E. postvittana males captured in sex pheromone traps.

Material and Methods

STUDY SITES

The Azorean archipelago stretches out over 615 km in the North Atlantic Ocean (37-40º N, 25-31º W), 1,584 km west of southern Europe, and 3,900 km east of the North American continent. It comprises nine main islands of recent volcanic origin, distributed in three groups: the western group of Corvo and Flores; the central group of Faial, Pico, Graciosa, São Jorge, and Terceira; and the eastern group of São Miguel and Santa Maria.

The current study was performed in São Miguel Island, the largest island in the archipelago of the Azores, with a surface area of 750 km².

To determine the temporal profile of larvae abundance in eight host plants (Table 1), 30 plants of each endemic host species were randomly observed on a weekly basis. One leaf from each plant were collected (with or without larvae if the plant is damage or not) to be analyzed after that in laboratory, in both nurseries at Furnas (37º 46’ 37.790” N -25º 18’ 46.193” W) and Nordeste (37º 49’ 45.128” N -25º 08’ 54.289” W), in São Miguel island. The samplings program occurred during two years between April 2018 and December 2019.

In addition, two populations were monitored weekly from April to December 2019 (total of 31 weeks), using open-sided delta traps baited with a synthetic female sex pheromone lure (containing: E11-14Ac, E9E11-14Ac) to attract males. The numbers of male individuals caught in each trap was recorded weekly. Pheromone lures were replaced once a month in each trap per local between April and December 2019.

STATISTICAL ANALYSIS

Before data analysis, given high number of zeros, the number of observed larvae were (x+0.5) transformed to homogenize the variance (ZAR, 2010). None of the data were normally distributed (Shapiro-Wilk test, p < 0.05) and did not meet homogeneity of variance assumptions (Levene’s test, p < 0.05). Thus, analyses were performed using nonparametric Mann-Whitney U and/or Kruskal-Wallis H tests. In the last case, when significant differences were found, multiple comparisons were performed with unpaired two-samples Mann-Whitney U test applying the Bonferroni correction. All statistical tests were performed using ISPSS® Statistics v. 27, and the significance level was set at = 0.05.

Results and Discussion

The endemic plants reared in the Furnas and Nordeste nurseries, were attacked mainly by two lepidopteran species, being mostly E. postvittana (2018: 88.9%, 2019: 99%) and, to a minor percentage, Palpita vitrealis (Walker, 1863) (Lepidoptera: Crambidae) (2018: 12.5%, 2019: 1%). The latter species strongly and exclusively attacked Pau-branco in both nurseries (Furnas: 10.3%, Nordeste: 16.3%), the pattern of which was similar in both years of the survey.

A total of 827 plants attacked by E. postvittana were observed in Furnas nursery (2018: 503, 2019: 324) and 1227 in the Nordeste (2018: 649, 2019: 578), including the presence of 525 larvae distributed by the Furnas (2018: 178 (35.4%), 2019: 79 (20.2%)) and from the Nordeste (2018: 131 (24.4%), 2019: 137 (23.70%)) (Table 2, Fig. 2).

Concerning the weekly average abundance of larvae, in 2018, at Furnas nursery it was highest in Ginja (mean ± SE: 2.79 ± 0.577 larvae), Faia (1.35 ± 0.249) and Sanguinho (0.71 ± 0.172), while in the Nordeste it was in Faia (1.38 + 0.280), Sanguinho (0.77 ± 0.174) and Pau-branco (0.5 ± 0.175). In 2019, the highest number of larvae was observed at Furnas in Faia (0.73 + 0.139), Sanguinho (0.75 ± 0.205) followed by Pau-branco (0.38 ± 0.122), while in the Nordeste it was in Ginja (1.81 ± 0.436) followed by Sanguinho (0.94 ± 0.240) and Faia (0.50 ± 0.095). In both the Furnas and Nordeste nurseries, during the two years of observations, Urze, Cedro, Folhado and Azevinho showed a very low average weekly number of larvae (< 0.1 larvae). At the Furnas nursery in 2019, unlike in 2018, the number of larvae found on Ginja was very low due to the small number of plants in production (Fig. 3).

The weekly mean abundance of E. postvittana larvae only varied significantly for overall host plants during both years of observations on Ginja (Kruskal-Wallis [KW]: x² = 35,393; df = 3; p = 0,000) and Azevinho (KW: x² = 10,178, df = 3; p = 0,017). Comparing annual larval abundance on Ginja, we found a significant difference only for the Furnas 2018/Furnas 2019 (Mann-Whitney U test: Z = -46.225, p = 0.000), Furnas 2018/Nordeste 2018 (Z = 33.309, p = 0.001) and Furnas 2019/Nordeste 2019 (Z = - 31.963, p = 0.000).

The larval abundance was relatively low at both locations and seems to be dependent on the density of their host plants in production and may show a distinct profile variation from year to year. Although E. postvittana fed on all eight nursery-grown plants, it showed a greater preference for young plants of Faia, Sanguinho and Ginja (Fig. 3).

Table 3 shows that the mean weekly abundance of E. postvittana males captured in the sex pheromone traps between May and December 2019 (total 31 weeks) was higher at the Furnas nursery (76.14%) than at the Nordeste (23.86%) (Z = -1.960; p = 0.05). However, it was observed that the pattern of adult distribution is relatively similar for both sites (Fig. 4).

The results of the average weekly abundance of E. postvittana males seems to indicate overlapping generations depending on the presence/absence of host plants in production (Figs 3 and 4), under relatively stable abiotic conditions, but maintaining the pattern of abundance throughout the year at both larval and adult levels. As observed for continental regions, particularly in Australia (ZIELONKA et al., 2021) and USA - California (BUERGI, 2012), there are at least 3 to 4 annual peaks in the abundance of larvae and adults, suggesting that the populations on São Miguel island appear to undergo at least three to four generations annually; also, adults are active year-round, and there is no winter resting stage.

Conclusions

Our results provide preliminary information on population dynamics of E. postvittana in the Azores, including the temporal profile of larval abundance in seven endemic host plants and one native species grown in two forest nurseries of the São Miguel Island (Furnas and Nordeste) and the abundance of males captured in sex pheromone traps.

The results suggests: (i) the population density varied throughout the year and as a function of the host plant species provided; (ii) the abundance profile in São Miguel Island indicates at the occurrence of at least three to four generations per year and that adults are active year-round, experiencing some delayed development during the winter; (iii) a low larval density does not represent very serious damage to Azorean endemic plants, but is reflected in the population density of its natural enemies; (iv) some biological control agents are present in the field, parasitizing the larvae (i.e. Braconidae species of Meteorus ictericus (Nees, 1811) and Microgaster opheltes Nixon, 1968); (v) finally, the knowledge of population dynamics and its natural enemies needs further and long-term study.

Acknowledgments

This research was support by Oficial Forestry Services from Regional Government of the Azores, through the research project MoCIL “Monitorização e Controlo Integrado de Lepidópteros em Viveiros Florestais (Nordeste e Furnas) na ilha de São Miguel - Açores”, in direct collaboration with the Forestry Engineers Carina Nóbrega and Catarina Quintela. Special thanks are due to laboratory technician Manuel Fernando Almeida for their help in the field work.

BIBLIOGRAPHY

ADLER, C. R. L.,1991.– Identification of pupae on apple in eastern North America, Pp. 51-64.– In L. P. S. VAN DER GEEST & H. H. EVENHUIS (Eds). Tortricid pests: their biology, natural enemies and control: 808 pp. Elsevier, Amsterdam.

BORGES, P. A. V., REUT, M., PONTE, N. B. DA, QUARTAU, J. A., FLETCHER, M., SOUSA, A. B., POLLET, M., SOARES, A. O., MARCELINO, J. A. P., REGO, C. & CARDOSO, P., 2013.– New records of exotic spiders and insects to the Azores, and new data on recently introduced species.– Arquipelago. Life and Marine Sciences, 30: 57-70.

BROCKERHOFF, E. G., SUCKLING, D. M., ECROYD, C. E., WAGSTAFF, S. J., RAABE, M. C., DOWELL, R. V. & WEARING, C. H., 2011.– Worldwide host plants of the highly polyphagous, invasive Epiphyas postvittana (Lepidoptera: Tortricidae).– Journal of Economic Entomology, 104: 1514-1524. DOI:10.1603/ EC11160.

BROWN, J. W., EPSTEIN, M. E., GILLIGAN, T. M., PASSOA, S. C. & POWELL, J. A., 2010.– Biology, identification, and history of the light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae: Archipini).– American Entomologist, 56: 34-43.

BUERGI, L. P., 2012.– Abiotic and biotic factors affecting light brown apple moth, Epiphyas postvittana, in California. PhD Thesis at University of California, Berkeley. Available from: https://escholarship.org/content/qt8w02g9n8/qt8w02g9n8_noSplash_4ffbe99214bfd612a9427f241cd8826c.pdf?t=mtfe8i.

CABI, 2021.– Epiphyas postvittana (light brown apple moth). Available from: https://www.cabi.org/isc/datasheet/54204.

CARDOSO, P., ARNEDO, M. A., TRIANTIS, K. A. & BORGES, P. A. V., 2010.– Drivers of diversity in Macaronesian spiders and the role of species extinctions.– Journal of Biogeography, 37: 1034-1046. Doi:10.1111/ j.1365-2699.2009.02264.x.

DANTHANARAYANA, W., 1975.– The bionomics, distribution and host range of the light brown apple moth, Epiphyas postvittana (Walk.) (Tortricidae).– Australian Journal of Zoology, 23(3): 419-437.

GBIF, 2021.– Epiphyas postvittana (Walker, 1863). Available from: https://www.gbif.org/pt/species/1737131.

HOGG, B. N., WANG, X. G., LEVY, K., MILLS, N. J. & DAANE, K. M., 2013.– Complementary effects of resident natural enemies on the suppression of the introduced moth Epiphyas postvittana.– Biological Control, 64: 125-131.

MOREY, A., 2015.– Phenotypic variation in cold tolerance of an invasive insect (Epiphyas postvittana Walker): Implications for forecasting risk.– Retrieved from the University of Minnesota Digital Conservancy. Available from: https://hdl.handle.net/11299/177124.

PÉREZ SANTA-RITA, J. V., ROS-PRIETO, A., VIEIRA, V., KARSHOLT, O., GABRIEL, R. & BORGES, P. A. V., 2018.– New records of moths (Insecta, Lepidoptera) from urban gardens on Terceira Island with new data on recently introduced species to the Azores.– Arquipelago. Life and Marine Sciences, 35: 47-65.

ROSAGRO, R. M., BORGES, I., VIEIRA, V., PONS SOLÉ, G. & SOARES, A. O., 2019.– Evaluation of Scymnus nubilus (Coleoptera: Coccinellidae) as biological control agent against Aphis spiraecola and Cinara juniperi (Hemiptera: Aphididae).– Pest Management Science, 76: 818-826.

SUCKLING, D. & BROCKERHOFF, E., 2010.– Invasion Biology, Ecology, and Management of the Light Brown Apple Moth (Tortricidae).– Annual review of entomology, 55: 285-306.

TERZOPOULOU, S., RIGAL, F., WHITTAKER, R. J., BORGES, P. A. V. & TRIANTIS, K. A., 2015.– Drivers of extinction: the case of Azorean beetles.– Biology Letters, 11: 1-4. DOI:10.1098/rsbl.2015.0273.

THOMAS, W. P., 1975.– Additional notes on leaf rollers.– Orchardist of New Zealand, 48(10): 354-355.

TRIANTIS, K. A., BORGES, P. A. V., LADLE, R. J., HORTAL, J., CARDOSO, P., GASPAR, C., DINIS, F., MENDONÇA, E., SILVEIRA, L. M. A., GABRIEL, R., MELO, C., SANTOS, A. M. C., AMORIM, I. R., RIBEIRO, S. P., SERRANO, A. R. M., QUARTAU, J. A. & WHITTAKER, R. J., 2010.– Extinction debt on oceanic islands.– Ecography, 33: 285-294. DOI: 10.1111/j.1600-0587.2010.06203.x.

VIEIRA, V. & KARSHOLT, O., 2010.– Lepidoptera.– In P. A. V. BORGES, A. COSTA, R. CUNHA, R. GABRIEL, V. GONÇALVES, A. F. MARTINS, I. MELO, M. PARENTE, P. RAPOSEIRO, P. RODRIGUES, R. S. SANTOS, L. SILVA, P. VIEIRA & V. VIEIRA (eds.).– A list of the terrestrial and marine biota from the Azores: 432 pp. Princípia, Oeiras.

VIEIRA, V., MOURA, M. & SILVA, L., 2020.– Terrestrial Flora of the Azores - A Field Guide: 336 pp. Letras Lavadas Edições, Ponta Delgada.

VIVES MORENO, A., 2014.– Catálogo sistemático y sinonímico de los Lepidoptera de la Península Ibérica, de Ceuta, de Melilla y de las Islas Azores, Baleares, Canarias, Madeira y Salvajes (Insecta: Lepidoptera): 1184 pp. Suplemento de SHILAP Revista de lepidopterología. Improitalia, Madrid.

WANG, X. G., LEVY, K., MILLS, N. J. & DAANE, K. M., 2012.– Light brown apple moth in California: a diversity of host plants and indigenous parasitoids.– Environmental Entomology, 41(1): 81-90. Available from: http://esa.publisher.ingentaconnect.com/content/esa/envent/2012/00000041/00000001/art00009.

WEARING, C. H., THOMAS, W. P., DUGDALE, J. S. & DANTHANARAYANA, W., 1991.– Tortricid pests of pome and stone fruits, Australian and New Zealand species, pp. 453- 472.– In L. P. S. VAN DER GEEST & H. H. EVENHUIS (Eds). Tortricid pests: their biology, natural enemies, and control: 808 pp. Elsevier, Amsterdam.

ZAR, J. H., 2010.– Biostatistical Analysis (5th ed.): 960 pp. Prentice-Hall/Pearson: Upper Saddle River, N. J.

ZIELONKA, M. W., HARRIS, W. E., POPE, T. W. & LEATHER, S. R., 2021.– Abundance and phenology of two pest species, Cacoecimorpha pronubana and Epiphyas postvittana (Lepidoptera: Tortricidae).– Annals of Applied Biology, 179: 207-215. Available from https://doi.org/10.1111/aab.12692.

Notas de autor

virgilio.ff.vieira@uac.pt