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- Evaluation of Scymnus nubilus (Coleoptera : Coccinellidae) as a biological control agent against Aphis spiraecola and Cinara juniperi (Hemiptera: Aphididae)Publication . Rosagro, Roberto Meseguer; Borges, Isabel; Vieira, Virgilio; Solé, Gemma Pons; Soares, António O.Aphids are a major insect pest of forestry systems. In this study, we evaluate the potential of the ladybeetle Scymnus nubilus Mulsant (Coleoptera: Coccinellidae) as a biological control agent against Aphis spiraecola Patch and Cinara juniperi (De Geer) (Hemiptera: Aphididae) infesting Azorean endemic plants reared in forestry nurseries.
- Exotic ladybirds for biological control of herbivorous insects : a reviewPublication . Rondoni, Gabriele; Borges, Isabel; Collatz, Jana; Conti, Eric; Costamagna, Alejandro C.; Dumont, François; Evans, Edward W.; Grez, Audrey A.; Howe, Andy G.; Lucas, Éric; Maisonhaute, Julie‐Éléonore; Soares, António O.; Zaviezo, Tania; Cock, Matthew J. W.Since the late 19th century, exotic ladybirds (Coleoptera: Coccinellidae) have been used extensively for suppressing herbivorous insects of economic importance. In recent decades, the introduction of non-native biological control (BC) agents has been greatly limited due to the awareness of the potential non-target effects of introductions. Nonetheless, recent episodes of biological invasions of economically important pests have raised the need to carefully consider whether the expected benefits of pest control go beyond the possible environmental risks of introduction. To better understand the factors that contributed to successful BC programs, here we review the literature behind classical and augmentative BC using exotic ladybirds. Additionally, by means of case studies, we discuss the BC efficacy of selected exotic species, e.g., Coccinella septempunctata L., Harmonia axyridis (Pallas), and Hippodamia variegata (Goeze), and their position within the communities of predators in the introduced areas of USA, Canada, and Chile. In Europe, much of the research on exotic ladybirds has been conducted on the undesired impact of H. axyridis. Therefore, we summarize the risk assessment data for this species and review the field research investigating the ecological impact on European aphidophagous predators. According to the BIOCAT database of classical BC programs, 212 ladybird species belonging to 68 genera have been released in about 130 years of BC activity, with 14.6% of introductions having resulted in partial, substantial, or complete control of the target pest. However, because post-release evaluation of establishment and BC success has not always been conducted, this rate could underestimate the successful cases. Among other factors, ladybird establishment and pest suppression mostly depend on (1) intrinsic factors, i.e., high voracity, synchronized predator-prey life cycle, and high dispersal ability, and (2) extrinsic factors, i.e., adaptability to the new environment and landscape composition. This review contributes to improved understanding of ladybirds as exotic BC agents.
- Abundance of Tuta absoluta (Meyrick, 1917) and its natural enemies on tomato crops in greenhouses of different production modes (Azores, Portugal) (Lepidoptera: Gelechiidae)Publication . Oliveira, Luísa; Borges, Isabel; Silva, Dário; Durão, Ana C.; Soares, António O.Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) is a major pest of tomato (Solanum lycopersicum L.) crops produced in the Azorean greenhouses. Despite the major concerns, no systematic study is available to describe population dynamics of T. absoluta and its natural enemies. The objective of this study was to compare the abundance of the pest (eggs and larvae) and its native natural enemies, in greenhouses of tomato crops produced under different production modes (biological, traditional and intensive). A sampling program was carried out during 2020-2021 and two production seasons of spring-summer and fall-winter. The abundance of eggs and larvae of T. absoluta were higher in tomato crops in intensive production and lower in biological production mode. Infestations by eggs and larvae were higher in spring-summer seasons. The natural enemies recorded were Macrolophus pygmaeus (Rambur, 1839) (Hemiptera: Miridae), Dicyphus cerastii Wagner, 1951 (Hemiptera: Miridae) and Trichogramma achaeae Nagaraja & Nagarkatti, 1960 (Hymenoptera: Trichogrammatidae). The abundance of natural enemies were very low and, virtually, do not occur during the fall-winter seasons. We found no significant difference between the abundance of M. pygmaeus amongst tomato crops from different production mode but D. cerastii was more abundant on greenhouses of biological production mode. Parasitism rate by T. achaeae does not differ between production modes and crop seasons. Considering the major concerns of the growers by the infestation levels of their crops, together with low abundance of native natural enemies, we suggest the use of biological production mode or an inoculative or augmentative strategy to control the pest in intensive and traditional productions modes.
- Eden Arthropod Azores DatabasePublication . Marcelino, Jose; Borges, Paulo A. V.; Borges, Isabel; Soares, António O.This study intended to contribute to the current international directives concerning biodiversity, aiming to document and safeguard biological resources of the globe. Our objective was to present the most widely distributed and diverse taxa recorded during the sampling phase of the EDEN project (2008-2014), specifically all arthropod fauna, at all strata, within eight representative habitats of five islands of the Azores archipelago (Santa Maria, São Miguel, Terceira, Flores and Pico)
- Diversity of Lepidoptera recorded in a forest nursery of Nordeste county on São Miguel Island (Azores)Publication . Vieira, Virgilio; Oliveira, Luísa; Soares, António O.; Borges, Paulo A. V.; Borges, Isabel; Tavares, JoãoThe diversity of moth species (Insecta, Lepidoptera) recorded in the forest nursery of Nordeste county on São Miguel island (Azores) is given. Adults were sampled between March and December 2019 using three methods: (i) light trap to caught Noctuidae species, (ii) open-sided delta trap baited with a synthetic female sex pheromone lure to attract Epiphyas postvittana males and (iii) entomological net to identify microlepidopteran moths. A total of 10160 adults belonging to 33 lepidopteran species were recorded and listed by families, including: Argyresthiidae 1 (3%), Crambidae 4 (12%), Erebidae 1 (3%), Geometridae 5 (15%), Noctuidae 18 (55%), Sphingidae 1 (3%), Tineidae 1 (3%), and Tortricidae 2 (6%). The families Noctuidae, Geometridae and Crambidae were the most diverse. Those with the highest abundance of adults was the Noctuidae family followed by the Crambidae, Trotricidae and Tineidae. The number of caught adults was consistently higher during spring and summer, decreasing sharply in late fall. For 14 species caught in the light trap the adult sex ratio was favorable to females, except for Xestia c-nigrum which was favorable to males. An analysis of the colonization status, feeding and primary hosts of these endemic, native or exotic moth species suggests that plants reared in forest nurseries, being attacked by such insects, facilitates our understanding of the diversity of lepidopterans that establish in Laurel Forest environments and to what extent there is a need to monitor and control them mainly with biological control agents.
- An updated checklist to the biodiversity data of ladybeetles (Coleoptera: Coccinellidae) of the Azores Archipelago (Portugal)Publication . Soares, António O.; Borges, Isabel; Calado, Hugo Renato; Borges, Paulo A. V.BACKGROUND: A recently-published review from 2021 presents a comprehensive checklist of ladybeetles of Portugal, including the Azores and Madeira Archipelagos. Until then, the available information was very scattered and based on a single revision dating back to 1986, a few international catalogues and databases, individual records and studies on communities of agroecosystems. However, no information was available on faunal composition across the Azorean islands and their habitats, using standardised inventories. Here, we present data about the biodiversity of ladybeetles and their distribution and abundance in five Islands of the Azores (Faial, Graciosa, Pico, São Jorge and São Miguel). Surveys included herbaceous and arboreal habitats from native to anthropogenic-managed habitats: ruderal road vegetation, vegetable garden, mixed forest of endemic and non-native host plants, coastal prairies, coastal mixed vegetation, cornfields and urban areas. We aimed to contribute to the ongoing effort to document the terrestrial biodiversity of Portugal, including the Archipelago of the Azores, within the research project AZORESBIOPORTAL–PORBIOTA (ACORES-01-0145-FEDER-000072). NEW INFORMATION: In this study, a total of 1,487 specimens of Coccinellidae belonging to 19 species are reported for several habitats. The listed species are from one single sub-familiy (Coccinellinae) and six tribes; Chilocorini (one species), Coccidulini (three species), Coccinellini (six species), Noviini (one species), Scymnini (seven species), Stethorini (one species). The number of species collected per island differed; Faial (10 species), Graciosa (four species), Pico (seven species), São Jorge (seven species) and São Miguel (12 species). For six species, new island records are given. Currently, the number of species known to occur in the Azores are 32, including two doubtful records. The majority of species are Scymnini, being Scymnus (Scymnus) interruptus (Goeze, 1777) and Scymnus (Scymnus) nubilus Mulsant, 1850, the most abundant species (relative abundance 71.1%). This database will be the baseline of a long-term monitoring project allowing assessment of the impact of ongoing global changes in the distribution and abundance of ladybeetles.
- A roadmap for ladybird conservation and recoveryPublication . Soares, António O.; Haelewaters, Danny; Ameixa, Olga M. C. C.; Borges, Isabel; Brown, Peter M. J.; Cardoso, Pedro; de Groot, Michiel D.; Evans, Edward W.; Grez, Audrey A.; Hochkirch, Axel; Holecová, Milada; Honěk, Alois; Kulfan, Ján; Lillebø, Ana I.; Martinková, Zdenka; Michaud, J. P.; Nedvěd, Oldřich; Omkar, null; Roy, Helen E.; Saxena, Swati; Shandilya, Apoorva; Sentis, Arnaud; Skuhrovec, Jiří; Viglášová, Sandra; Zach, Peter; Zaviezo, Tania; Losey, John E.Ladybirds (Coleoptera: Coccinellidae) provide services that are critical to food production, and they fulfill an ecological role as a food source for predators. The richness, abundance, and distribution of ladybirds, however, are compromised by many anthropogenic threats. Meanwhile, a lack of knowledge of the conservation status of most species and the factors driving their population dynamics hinders the development and implementation of conservation strategies for ladybirds. We conducted a review of the literature on the ecology, diversity, and conservation of ladybirds to identify their key ecological threats. Ladybird populations are most affected by climate factors, landscape composition, and biological invasions. We suggest mitigating actions for ladybird conservation and recovery. Short-term actions include citizen science programs and education, protective measures for habitat recovery and threatened species, prevention of the introduction of non-native species, and the maintenance and restoration of natural areas and landscape heterogeneity. Mid-term actions involve the analysis of data from monitoring programs and insect collections to disentangle the effect of different threats to ladybird populations, understand habitat use by taxa on which there is limited knowledge, and quantify temporal trends of abundance, diversity, and biomass along a management-intensity gradient. Long-term actions include the development of a worldwide monitoring program based on standardized sampling to fill data gaps, increase explanatory power, streamline analyses, and facilitate global collaborations.
- Standardised arthropod (Arthropoda) inventory across natural and anthropogenic impacted habitats in the Azores archipelagoPublication . Marcelino, José; Borges, Paulo A. V.; Borges, Isabel; Pereira, Enésima; Santos, Vasco; Soares, António O.BACKGROUND In this paper, we present an extensive checklist of selected arthropods and their distribution in five Islands of the Azores (Santa Maria. São Miguel, Terceira, Flores and Pico). Habitat surveys included five herbaceous and four arboreal habitat types, scaling up from native to anthropogenic managed habitats. We aimed to contribute to the ongoing effort to document the terrestrial biodiversity of the world, in particular the Portuguese archipelago of the Azores, as islands harbour a significant portion of unique terrestrial biodiversity. Selection of Arthropoda groups for the current checklist was based on their known richness and abundance (Arachnida, Collembola, Hemiptera, Neuroptera, Coleoptera, Hymenoptera), in almost all terrestrial ecosystems, as well as their importance in current Integrated Pest Management and alternative Biocontrol protocols at large (i.e. hymenopteran parasitoids and beneficial Coleoptera). In addition, we include the list of Dermaptera, Orthoptera, Psocoptera and Thysanoptera species. These assembled groups represent part of the monitoring programme EDEN Azores (2008-2014), where all Arthropod fauna, at all strata, within nine representative habitats of the abovementioned five Islands of the Azores was recorded. NEW INFORMATION In this study, a total of 116,523 specimens, belonging to 483 species and subspecies of selected groups of arthropods, are reported by order, family and, when possible, genus and species. Hymenopteran, mostly parasitoids, accounted for the most represented taxa across all the monitoring and sampling phase of EDEN Azores (193 species and mophospecies), followed by Coleoptera (95 species); Collembola (89 species); and Araneae (72 species). A total of 37 non-native species are reported for the first time in the Azores. Coleoptera: Asaphidion flavipes (Linnaeus, 1761) (Carabidae); Tachyporus dispar (Paykull, 1789) (Staphylinidae). Hemiptera: Acrosternum heegeri Fieber, 1861 (Pentatomidae). Collembola: Entomobrya regularis Stach, 1963 (Entomobryidae); Lepidocyrtus lusitanicus piezoensis (Simón-Benito, 2007) (Entomobryidae); Jordanathrix articulata (Ellis, 1974) (Sminthuridae); Sminthurinus quadrimaculatus (Ryder, 1879) (Katiannidae); Himalanura sp. (Entomobryidae); Protophorura sp. (Onychiuridae). Hymenoptera, parasitoids: Aphidius colemani Viereck, 1912 (Braconidae); Aphidius ervi Haliday, 1834 (Braconidae); Aphidius matricariae Viereck, 1912 (Braconidae); Aphidius rhopalosiphi Stefani-Perez, 1902 (Braconidae); Aphidius rosae (Haliday, 1834) (Braconidae); Aphidius urticae Haliday, 1834 (Braconidae); Centistidea ectoedemiae Rohwer, 1914 (Braconidae); Meteorus unicolor (Wesmael, 1835) (Braconidae); Meteorus collaris (Spin.) Hal. – Ruschka, Fulmek, 1915 (Braconidae); Orthostigma cratospilum (Thomson, 1895) (Braconidae); Orthostigma latriventris Ratzeburg, 1844 (Braconidae); two other species of Orthostigma sp.; Pseudopezomachus bituberculatus (Marshall, 1905) (Braconidae); Tanycarpa punctata (van Achterberg, 1976) (Braconidae); Gonatopus clavipes (Thunberg, 1827) (Dryinidae). New genera not previously recorded for the Azores include: Pycnetron sp. (Chalcidoidea: Pteromalidae); four species of Aspilota sp. (Braconidae: Alysiinae); four species of Chorebus sp. (Braconidae: Aphidiinae: Alysiinae); Microgaster sp. (Braconidae: Microgastrinae); Homolobus sp. (Braconidae: Homolobinae); Lodbrokia sp. (Braconidae: Alysiinae). These 37 taxa were found in several Islands and five are new species for Flores Island, 10 species are new for Pico Island, 12 species are new for Terceira Island, 19 species are new for S. Miguel Island and five species are new for S. Maria Island. Additional species records for the Islands included: Flores (5 Collembola, 9 Araneae; 2 Hemiptera; 8 Coleoptera, 8 Hymenoptera), Pico (4 Collembola; 7 Araneae; 4 Hemiptera; 11 Coleoptera; 9 Hymenoptera), Terceira (4 Collembola; 1 Araneae; 3 Hymenoptera), S. Miguel (1 Araneae; 2 Coleoptera; 3 Hymenoptera), S. Maria (5 Collembola; 3 Araneae; 2 Hemiptera; 2 Hymenoptera).
- Abundance of Epiphyas postvittana (Walker, 1863) in forestry nurseries of São Miguel Island (Azores, Portugal) (Lepidoptera: Tortricidae)Publication . Oliveira, Luísa; Vieira, Virgilio; Soares, António O.; Borges, Isabel; Arruda, Patrícia Melo; Tavares, JoãoEpiphyas postvittana (Walker, 1863) is an invasive polyphagous pest for the Azores and its bioecology and the potential natural enemies were unknown. We evaluated the temporal profile of this species larval abundance and the number of males captured in sex pheromone traps, hypothesizing that both profiles were similar. The study was carried out on seven endemic host plants and one native species grown in two forest nurseries (Furnas and Nordeste) in São Miguel Island over two years from 2018 to 2019. 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, 2019: 79) and from the Nordeste (2018: 131, 2019: 137). In 2019, the average weekly number of males captured in the sex pheromone traps (total 31 weeks) were higher in Furnas (mean ± SE: 9.68 ± 1.982) than in Nordeste (3.33 ± 0.651). In synthesis, (i) the population density varied throughout the year and as a function of the host plant species in production; (ii) the abundance profile of larval and adults suggests has 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 the population dynamics and its natural enemies needs further and long-term study.
- Can the ladybird predator Scymnus nubilus contribute to control of the aphid Aphis frangulae, a pest threatening the Macaronesia endemic Frangula azorica?Publication . Borges, Isabel; Arruda, Patrícia Melo; Meseguer, Roberto; Vieira, Virgilio; Pons-Solé, Gemma; Soares, António O.Aphis frangulae (Hemiptera: Aphididae) is a major pest of the laurel forest endemic Frangula azorica (Rosales: Rhamnaceae) produced in nursery conditions by the Forestry Services of the Azores (Portugal). The suitability of A. frangulae for the development and reproduction of a potential biological control agent, Scymnus nubilus (Coleoptera: Coccinellidae), was assessed under laboratory conditions (25 ± 1 °C, 75 ± 5% RH, 16:8 L:D photoperiod). The predation potential of S. nubilus was also assessed. Scymnus nubilus 4th instar larvae and pupae successfully completed development in 9.0 ± 0.2 days. The 4th instar larvae ate 15.1 aphids per day, corresponding to 1.52 mg of biomass ingested. On A. frangulae, S. nubilus females took 5.5 ± 0.3 days to start oviposition and an average of 135 ± 12 eggs were laid per female over the first 15 days of oviposition. Field tests showed that S. nubilus 4th instar larvae were more efficient in controlling the pest in closed systems (isolated aphid colonies) and the effect was more pronounced at high predator densities within three days. In open systems, the aphid natural control was higher than initially expected. This work highlights the role of the large aphidophagous guild present in forestry nurseries. The results of this study show that A. frangulae is an essential prey species for S. nubilus and therefore the predator can be used in pest management programs against this pest. However, further studies focusing on different biological control tactics (inundative or inoculative) are required to assess more accurately the effectiveness of S. nubilus as a biological control agent against A. frangulae.
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