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(Heteroptera: Thaumastocoridae) at Different Temperatures www.nature.com/scientificreports OPEN Biological parameters, life table and thermal requirements of Thaumastocoris peregrinus Received: 2 July 2018 Accepted: 11 April 2019 (Heteroptera: Thaumastocoridae) Published: xx xx xxxx at diferent temperatures L. R. Barbosa1, F. Santos2, E. P. Soliman3, A. P. Rodrigues1, C. F. Wilcken3, J. M. Campos4, A. J. V. Zanuncio5 & J. C. Zanuncio6 Temperature afects the development, population dynamics, reproduction and population size of insects. Thaumastocoris peregrinus Carpintero et Dellape (Heteroptera: Thaumastocoridae) is a eucalyptus pest. The objective of this study was to determine biological and life table parameters of T. peregrinus on Eucalyptus benthamii at fve temperatures (18 °C; 22 °C; 25 °C; 27 °C and 30 °C) with a relative humidity (RH) of 70 ± 10% and photoperiod of 12 hours. The duration of each instar and the longevity of this insect were inversely proportional to the temperature, regardless of sex. The nymph stage of T. peregrinus was 36.4 days at 18 °C and 16.1 days at 30 °C. The pre-oviposition period was 5.1 days at 30 °C and 13.1 days at 18 °C and that of oviposition was 7.6 days at 30 °C and 51.2 days at 22 °C. The generation time (T) of T. peregrinus was 27.11 days at 22 °C and 8.22 days at 30 °C. Lower temperatures reduced the development and increased the life stage duration of T. peregrinus. Optimum temperatures for T. peregrinus development and reproduction were 18 and 25 °C, respectively. Te frequent introduction and establishment of exotic insect pests on eucalyptus plantations in Brazil are impact- ing and reducing productivity. Te bronze bug Taumastocoris peregrinus Carpintero & Dellapé (Hemiptera: Taumastocoridae), an Australian eucalyptus pest was frst recorded in Brazil in 20091. At high infestations, this insect decreases the photosynthetic rate, leading to partial or total plant defoliation, and in some cases, plant death2,3. Studies have focused on the biology4–6, chemical control7, chemical ecology8,9, morfology10, remote sensing for monitoring11,12 and biological control13–16 of this pest, aiming to minimize losses. However, the efect of temper- ature on the biological parameters of this species is not yet well known. Ambient temperature is one of the most important abiotic factors afecting the survival, development rate, abundance, behavior and ftness of insects17–20. In fact, each insect species has an optimum temperature at which they thrive, with lower and upper limits for development21,22. High temperatures can decrease fecundity, hatch- ing and survival of these organisms23, while low temperatures can afect the sex ratio (reduce male proportion), behavior, and population distribution of insects24. Te study of temperature in life-history variables, such as nymph development period, adult longevity and fecundity is crucial to the development of pest-management strategies25. Te temperature decrease Parapoynx crisonalis (Lepidoptera: Pyralidae) life tables26 and Brachmia macroscopa (Lepidoptera: Gelechiidae) development 1Empresa Brasileira de Pesquisa Agropecuária- Embrapa Florestas, 83411-000, Colombo, Paraná, Brazil. 2Departamento de Entomologia e Acarologia, Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, 13418-900, Piracicaba, São Paulo, Brazil. 3Departamento de Proteção Vegetal, Faculdade de Ciências Agronômicas, Universidade Estadual Paulista “Júlio de Mesquita Filho”, 18610-307, Botucatu, São Paulo, Brazil. 4Departamento de Fitotecnia, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil. 5Departamento de Engenharia Florestal, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil. 6Departamento de Entomologia/BIOAGRO, Universidade Federal de Viçosa, 36570-900, Viçosa, Minas Gerais, Brazil. Correspondence and requests for materials should be addressed to L.R.B. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:10174 | https://doi.org/10.1038/s41598-019-45663-5 1 www.nature.com/scientificreports/ www.nature.com/scientificreports °C First instar Second Tird Fourth Fifh Ny-Ad. 6.79 ± 0.23a 6.30 ± 0.21a 6.02 ± 0.23a 6.93 ± 0.22ª 10.42 ± 0.31a 36.37 ± 0.26ª 18 °C n = 84 n = 75 n = 71 n = 63 n = 58 n = 52 6.46 ± 0.14a 5.59 ± 0.17a 5.97 ± 0.21a 6.02 ± 0.26b 8.78 ± 0.29b 32.47 ± 0.33b 22 °C n = 93 n = 82 n = 70 n = 63 n = 51 n = 36 4.561 ± 0.13b 3.82 ± 0.11b 4.05 ± 0.11b 4.24 ± 0.09c 6.15 ± 0.14c 22.69 ± 0.16c 25 °C n = 87 n = 81 n = 74 n = 65 n = 60 n = 52 4.07 ± 0.12c 3.45 ± 0.11b 3.58 ± 0.16c 3.90 ± 0.14c 5.34 ± 0.24 cd 20.0 ± 0.25d 27 °C n = 78 n = 71 n = 60 n = 52 n = 41 n = 33 3.45 ± 0.11d 2.81 ± 0.09c 2.69 ± 0.12d 2.97 ± 0.23d 4.43 ± 0.26d 16.13 ± 0.20e 30 °C n = 81 n = 77 n = 58 n = 45 n = 35 n = 23 Table 1. Duration (mean ± SE) of each instar and of the nymph period (days) (Ny-Ad.) of Taumastocoris peregrinus (Heteroptera: Taumastocoridae) reared at diferent temperatures, RH of 60 ± 10% and photoperiod 12:12 (L: D) h. Means followed by the same letter per line do not difer by the Tukey test (p ≤ 0.05). °C 18 °C 22 °C 25 °C 27 °C 30 °C N 20 11 20 13 8 Preov 13.10 ± 0.61ª 9.09 ± 0.41b 6.20 ± 0.24c 6.31 ± 0.59c 5.13 ± 0.55c Ovip. (days) 36.3 ± 3.8ab 51.2 ± 6.4b 29.9 ± 6.4a 21.5 ± 3.4a 7.6 ± 3.4c Eggs/female 45.9 ± 4.6ab 64.0 ± 9.08b 58.1 ± 8.5ab 49.08 ± 9.18ab 22.8 ± 12.5a Eggs/fem./day 1.1 ± 0.1ª 1.2 ± 0.09ab 1.6 ± 0.1bc 1.9 ± 0.19c 1.8 ± 0.4ac Fem. Long. (days) 41.84 ± 3.9cd 53.6 ± 6.2b 34.3 ± 3.6bc 24.69 ± 3.11ab 10.4 ± 3.4a Male Long. (days) 57.4 ± 3.4c 54.1 ± 7.0c 35.4 ± 1.8b 32.62 ± 3.29b 11.3 ± 2.9a Sex ratio* 0.48ª 0.58ª 0.48ª 0.53a 0.61a Table 2. Duration (mean ± SE) of the pre-oviposition (Preov.) and oviposition (Ovip.) (days), eggs per female (Eggs/female), eggs/female/day (Eggs/fem./day) and female (Fem. Long.) and male (Male Long.) longevity of Taumastocoris peregrinus (Heteroptera: Taumastocoridae) males and females at diferent temperatures, RH of 60 ± 10% and photoperiod 24:12 (L: D) h. Means followed by the same letter per line do not difer by Tukey test (p ≤ 0.05). and fecundity27. Tus, the objective of this study was to evaluate the efect of diferent temperatures on biological parameters of T. peregrinus. Results Nymph development. The nymph development period of T. peregrinus differed across temperatures (Kruskal-Wallis on ranks; df = 4, H = 168.42, P < 0.001) (Table 1). Furthermore, this parameter afected the dura- tion of each instar (frst-instar, Kruskal-Wallis on ranks; df = 4, H = 219.31, P < 0.001; second instar, Kruskal- Wallis on ranks; df = 4, H = 198.67, P < 0.001; third instar, Kruskal-Wallis on ranks; df = 4, H = 172.49, P < 0.001; fourth instar, Kruskal-Wallis on ranks; df = 4, H = 134.77, P < 0.001; and ffh instar, Kruskal-Wallis on ranks; df = 4, H = 126.4, P < 0.001) of this insect. Adult reproduction and longevity. Te pre-oviposition period of T. peregrinus decreased linearly with increased temperature, ranging from 13 (18 °C) to 5 (30 °C) days (Table 2). Te fertility of this insect was similar at 22 °C (64 eggs), 18 °C (45.9 eggs), 25 °C (58.1) and 27 °C (49.1), while it was lower at 30 °C (22 eggs) (Table 2). Female longevity of T. peregrinus was longest at 22 °C (53 days) and that of males at 18 to 22 °C (57 and 54 days, respectively) (Table 2). Temperature did not afect the sex ratio of this insect (GLM-binomial: χ2190 = 1.96, p = 0.74) (Table 2). Survival analysis. Temperature afected the survival rates of T. peregrinus nymphs (Mantel-Haenzel Test; χ2 = 53.6, P < 0·0001) (Fig. 1A), females (Mantel-Haenzel Test; χ2 = 60.9, P < 0·0001) (Fig. 1B), and males (Mantel-Haenzel Test; χ2 = 103, P < 0.0001) (Fig. 1C). Survival analysis using the Cox’s Proportional Hazards model showed a higher death risk (hazard ratio; HR) for nymphs and adults (females and males) of T. peregrinus as temperature increased (Table 3) and (Fig. 2). Threshold development and thermal constants. Te linear regression estimative for the tempera- ture limit of T. peregrinus frst, second, third, fourth and ffh instars was 7.70, 9.85, 10.33, 10.24 and 10.45 °C, respectively (Fig. 1). Te T. peregrinus thermal constant (K) per instar was 79.34 degree-day (DD) (frst), 58.58 DD (second), 55.57 DD (third), 62.24 DD (fourth) and 88.91 DD (ffh). Te accumulated temperature for the nymph-to-adult period of this insect was 338.50 DD, with a temperature limit of 9.93 °C (Fig. 1). Life table. Te net reproductive rate (R0) of T. peregrinus was higher at 25 °C (6.39) and 18 °C (4.45), the latter being similar to that at 22 °C (4.00). Te net reproduction rate was lower at 30 °C (0.13). Te generation time (T) SCIENTIFIC REPORTS | (2019) 9:10174 | https://doi.org/10.1038/s41598-019-45663-5 2 www.nature.com/scientificreports/ www.nature.com/scientificreports Figure 1. Relationship between temperature, development speed (1/days) of nymph and period of nymph- adult of Taumastocoris peregrinus (Heteroptera: Taumastocoridae), RH of 60 ± 10% and photoperiod 12:12 (L: D) h.____Development time (Days) Velocity of development (1/D).
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