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Thermal requirements and estimated number of generations of Neopamera bilobata (Say) in strawberry-producing regions of Brazil/Exigencias termicas e estimativa do numero de geracoes de Neopamera bilobata (Say) em regioes produtoras de morango do Brasil.


Most poikilothermic species are adapted to different temperature ranges, as temperature is a major factor influencing their geographic distributions (TRUDGILL et al., 2005). Thus, knowledge of the thermal requirements of a species is essential to predict its potential establishment in a given region (JAROSIK et al., 2015).

The effect of temperature on the dispersal and infestation intensity of a pest may affected by the physiological state of the insect or its host. By influencing natural mortality, changing plant-herbivore interactions, limiting the range of host plants, or altering their physiology, extreme temperatures restrict the size and geographical distribution of pest populations (BALE et al., 2002; KIRITANI, 2007; SPEIGHT et al., 2008; WHALEN & HARMON, 2015). Thus, understanding the effects of climate variation on insects is essential to predict the activity and density of insect pests or disease vectors (SPEIGHT et al., 2008). One example is Jadera haematoloma (Herrich-Schaeffer) (Heteroptera: Rhopalidae). This species is found in subtropical regions of the United States; since the 1980s, it has extended its range northward in response to milder temperatures and adaptation to different host plants (HOFFMAN & STEINER JR, 2005). For Umbonia crassicornis (Amyot & Serville) (Hemiptera: Membracidae), regular periods of below-freezing temperatures in northern Florida have been an effective barrier to prevent it from dispersing to this region (DOWELL & WOOD, 2014).

The direct influence of temperature on insect development can be measured by determining the thermal threshold and thermal constant. These parameters enable the development of predictive models for the occurrence of these insects (SILVEIRA NETO, 1976; SPEIGHT et al., 2008), such as those for the species Lygus hesperus Knight, L. rugulipennis Poppius, and L. lineolaris Palisot (Hemiptera: Miridae), pests of strawberries in the United States, United Kingdom, and Canada, respectively (BOSTANIAN et al., 1990; XU et al., 2014; UCDAVIS, 2015).

In Brazil, species of the genus Lygus do not cause yield losses in strawberry crops. However, the seed bug Neopamera bilobata (Say) (Hemiptera: Rhyparochromidae) has been recently reported in southern Brazil, feeding on unripe and ripe strawberry fruits and causing growth stunting, hardening, drying, and brown discoloration of pseudo fruits in early stages of infestation (BOTTON, 2016). These symptoms were described by BROOKS et al. (1929), who also noted that when infestation levels are high, the plant crown is also attacked, resulting in wilting.

To understand how populations of insects occur, several biological and abiotic factors must be evaluated, including the influence of temperature. For N. bilobata there is no information about the effect of this factor on development and population growth. This study was conducted to determine the thermal threshold and thermal requirements of N. bilobata and to estimate the number of generations of this species in the main strawberry-producing regions of Brazil.


The assay was conducted in the Laboratory of Entomology of Embrapa Uva e Vinho in Bento Goncalves, Rio Grande do Sul, in a climate chamber (B.O.D.) with 70 [+ or -] 10% relative humidity and 12h photophase.

Fruit materials

Strawberry fruits of the cultivar Aromas were harvested from plants grown in pots filled with 3L of soil, fertilized as recommended for the crop by CQFSRS/SC (2004), in a greenhouse. Two applications of Score[R] (40mL 100[L.sup.-1]), one of Vertimec 18 EC[R] (50mL 100[L.sup.-1]) and one of Karate Zeon 50 CS[R] (80mL 100[L.sup.-1]) were performed as phytosanitation treatments during the experiment, for the control of Mycosphaerella fragariae (Tul.) Lindau, Tetranychus urticae Koch and Chaetosiphon fragaefolii (Cockerell), respectively. Fruits were only used in the experiments after a minimum period of 30 or 15 days after the application of acaricides/insecticides or fungicides, respectively. A 10% milk solution was also applied weekly to control powdery mildew Sphaerotheca macularis (Wallr. ex Fr.) Jacz. f. sp. fragariae (EMBRAPA, 2006).

Insect origin

Insects used to start the laboratory colony were collected from strawberries 'Albion', in Caxias do Sul (29[degrees] 11' 49"S and 050[degrees] 57' 10"W), and of strawberries 'Aromas', in Farroupilha (29[degrees] 08' 15" S and 051[degrees] 24'30" W), Rio Grande do Sul.

Adult specimens were identified by Dr. Pablo Matias Dellape (National University of La Plata), who identified the target species as N. bilobata. Voucher specimens were deposited in the Padre Jesus Santiago Moure Museum (Universidade Federal do Parana, Curitiba, Parana) and in the Entomological Collection of Embrapa Uva e Vinho.

A colony was established at 25 [+ or -] 1[degrees]C, 12h photophase, as described by KUHN et al. (2014). Adults were maintained in 1L clear plastic containers (O 12cm x 9.5cm high), covered with perforated lids (4 x4cm) lined with voile fabric. For nymphs, the lid was replaced with plastic wrap. The bottom of the container was lined with paper towels to prevent excess moisture. Two ripe strawberry fruits of the cultivar Aromas were provided as food per container, and replaced twice a week.

Experimental design and data analysis

Ripe fruits of the cultivar Aromas were placed in containers with adult insects from the laboratory colony and examined after 24h for eggs, which were removed with the aid of a moistened brush. Eggs of known age were then transferred to unripe strawberry fruits, which were placed in individual 80ml cylindrical plastic containers (0 = 5cm x 6cm high) with two perforations on the lid (each 1.5cm in diameter), sealed with voile fabric attached with vinyl cement.

Six temperatures were examined (16, 19, 22, 25, 28, or 30 [+ or -] 1[degrees]C) and for each temperature, 120 eggs were used. A replicate consisted of one fruit and one egg. During development, nymphs were fed with unripe strawberry fruits (replaced twice a week) harvested from the greenhouse planting described above.

The development from egg to adult emergence was monitored daily. The mean durations and viabilities of the egg and nymph stages were calculated, and the duration values were compared with the Tukey test (P < 0.05). Based on the duration of each development stage, the estimated lower developmental threshold (T1) and the thermal constant (K) were determined with the Hyperbole method (HADDAD et al., 1999), from the equation of Reaumur:

K = D (T - T1)

K = Thermal constant; D = Development time (days);

T = Temperature at which the insect grew; T1 = lower developmental threshold

Therefore: 1/D = -T1/K + (1/K).T

Thus: Y = 1/D; a = -T1/K; b = 1/K; x = T

Obtaining the equation: Y = a + b.x

As by definition the insect stops developing at the lower developmental threshold (Y = 0): Tl = -a/b [degrees]C and K = 1/b DD (degree-days). To calculate the upper developmental threshold (Tu) (SILVEIRA NETO et al., 1976) the equation is: Tu = T1 + [square root of K].

The number of generations (NG) of N. bilobata per year was estimated based on the calculated Tl and K and historical monthly mean temperatures, where:

Cumulative degree-days = [[SIGMA].sub.(Jan-Dec)] N (Tm - Tl)

NG = Cumulative degree-days/K

N = number of days in the month, Tm = mean monthly temperature for each location, T1 = lower developmental threshold and K = thermal constant. Months with a lower mean monthly temperature than the lower developmental threshold were not included in the calculation of the cumulative degree-days.

Temperature data were selected from eight municipalities: Caxias do Sul (RS), Pelotas (RS), Jaboti (PR), Sao Jose dos Pinhais (PR), Atibaia (SP), Piedade (SP), Datas (MG), and Pouso Alegre (MG) (Brazilian state abbreviations: MG, Minas Gerais; PR, Parana; RS, Rio Grande do Sul; SP, Sao Paulo).

These municipalities were chosen because they are large strawberry producers in their regions (CARVALHO et al., 2014), and also because they have contrasting temperatures within the same region. For the municipalities of Sao Jose dos Pinhais, Jaboti, Datas, and Pouso Alegre, data from Curitiba, Joaquim Tavora, Diamantina, and Itajuba respectively were used, as they have similar climate conditions monitored by local meteorological stations. The mean monthly temperatures used were obtained from the Universidade Federal de Itajuba--UNIFEI (data used for Pouso Alegre), from the Center of Integrated Agrometereological Information CIIAGRO (for the municipalities of Atibaia and Piedade), Instituto de Agronomia do Parana IAPAR (for the municipality of Jaboti), and from the Insituto Nacional de Meteorologia (INMET) for the others.


N. bilobata did not complete its development at 16[degrees]C; only one individual reached the fourth instar (Table 1). The development time was longest at 19[degrees]C, with the second-lowest viability from egg to adult, indicating that this temperature is not suitable for growth of this species (Table 1).

The mean duration of the developmental stages of N. bilobata decreased as temperatures increased up to 28[degrees]C, while nymphal viability increased between 22 and 28[degrees]C (Table 1). These results support field observations reported by WILSON (1938), who described high infestations of N. bilobata in warmer periods. Field observations by GALLARDO-GRANADOS et al. (2016) in a protected crop area and open environment documented a population increase at the beginning of spring, favored by temperatures above 20[degrees]C.

At 30[degrees]C, the maximum temperature studied here, the development cycle lengthened, indicating that at this temperature, development may be compromised, as well as viability (11.11%), which was the lowest for the temperatures tested (Table 1).

The lowest Tl for the stages of N. bilobata was observed for the egg stage (13.1[degrees]C) and 121.8 degree-days were needed for the insect to complete this stage (Figure 1, table 2). The K values for N. bilobata instars ranged from 50.6 (2nd instar) and 80.6 (1st instar) degree-days, and 418.4 degree-days for the complete development (Table 2). Since this is the first study to determine the thermal requirements of N. bilobata, no comparative information is available. The K value obtained in our study was similar to the 140 and 346 degree-days reported by PICKEL et al. (1990) for the development of L. hesperus eggs and egg to adult, respectively; this species is a member of the same order, and causes damage to strawberry production in the United States.

The T1 observed for egg-to-adult development was 15.2[degrees]C (Table 2) and the upper threshold temperature (Tu) was 35.6[degrees]C, a thermal amplitude that matches with the cold and mild climates of the strawberry-producing regions in the country (CARVALHO et al., 2014).

Using the T1 and the thermal constant needed to complete the stages from egg to adult, the number of generations per year was estimated for the main strawberry-producing regions of Brazil (Figure 2). The highest number of generations was obtained for the municipality of Jaboti, Parana, with 5.1 generations/year, as opposed to Caxias do Sul, Rio Grande do Sul, with only 1.9 generations/year. These values demonstrate that most of the important strawberry-producing regions are suitable for the development of several generations of N. bilobata.

The estimated number of generations in the different strawberry-producing regions indicates where N. bilobata has the highest potential for population growth. Daily or weekly climate data in the different localities are useful for studies on predicting the occurrence and monitoring of pests. According to Integrated Pest Management (IPM) recommendations, the cultivation of any crop based on these concepts allows a rational use of resources and promotes economic and environmental sustainability (NORRIS et al., 2003). This approach can be used for the control of N. bilobata in Brazil, since similar strategies have been implemented elsewhere, such as for L. hesperus in strawberries in the United States (UCDAVIS, 2015).


The threshold temperature and thermal requirements of the seed bug Neopamera bilobata fed on strawberries are 15.2[degrees]C and 418.4 DD, respectively. N. bilobata can produce more than one generation annually, and is adapted to all Brazilian strawberry-producing regions.

Received 03.27.17 Approved 10.10.17


We thank Dr. Pablo Matias Dellape for insect identification, Cesar Ivan Suarez Castellanos for aid in data analysis, and Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Universidade Federal de Pelotas (UFPel) and Embrapa for financial support.


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Taciana Melissa de Azevedo Kuhn (1) * Alci Enimar Loeck (1) Marcos Botton (2)

(1) Programa de Pos-Graduacao em Fitossanidade, Faculdade de Agronomia Eliseu Maciel (FAEM), Universidade Federal de Pelotas (UFPel), 96010-900, Pelotas, RS, Brasil. E-mail: 'Corresponding author.

(2) Embrapa Uva e Vinho, Bento Goncalves, RS, Brasil.

Caption: Figure 1--Relationship between temperature, development time (*) and velocity of development (*) for egg and nymphal (1st, 2nd, 3rd, 4th, and 5th instar) stages and development cycle (egg-adult) of Neopamera bilobata fed unripe strawberry fruits of the cultivar Aromas at the temperatures of 16, 19, 22, 25, 28, or 30 [+ or -] 1[degrees]C (70 [+ or -] 10% RH; 12h photophase).
Table 1--Duration (mean [+ or -] SD) (days) and viability (%) of the
egg and nymphal stages and the development cycle (egg-adult) of
Neopamera bilobata fed unripe strawberry fruits of the cultivar Aromas
at the temperatures of 16, 19, 22, 25, 28, or 30 [+ or -] 1[degrees]C
(70 [+ or -] 10% RH; 12h photophase).

T        Parameter         Instar
rees]C                     Egg                   1st

         Duration (days)   33.3 [+ or -] 2.4 a   34.6 [+ or -] 8.8 a
16       Viability (%)     75.9                  9.8
         n1                (82)                  (8)
         Duration (days)   19.9 [+ or -] 1.7 b   19.2 [+ or -] 5.1 b
19       Viability (%)     67.0                  61.5
         n                 (65)                  (40)
         Duration (days)   16.8 [+ or -] 1.4 c   15.6 [+ or -] 4.3 c
22       Viability (%)     74.3                  66.7
         n                 (75)                  (50)
         Duration (days)   11.1 [+ or -] 1.7 d   8.2 [+ or -] 1.9 d
25       Viability (%)     74.1                  70
         n                 (80)                  (56)
         Duration (days)   7.8 [+ or -] 0.5 e    6.1 [+ or -] 1.3 d
28       Viability (%)     92.5                  86.8
         n                 (99)                  (86)
         Duration (days)   7.1 [+ or -] 0.3 f    5.9 [+ or -] 1.1 d
30       Viability (%)     57.3                  56.7
         n                 (67)                  (38)

T        Parameter         Instar
rees]C                     2nd                   3rd

         Duration (days)   20.0 a                25.0 a
16       Viability (%)     12.5                  100.0
         n1                (1)                   (1)
         Duration (days)   15.0 [+ or -] 6.3 a   16.2 [+ or -] 9.5 ab
19       Viability (%)     77.5                  77.4
         n                 (31)                  (24)
         Duration (days)   14.6 [+ or -] 5.5 a   14.0 [+ or -] 8.7 bc
22       Viability (%)     80                    72.5
         n                 (40)                  (29)
         Duration (days)   6.7 [+ or -] 2.9 b    5.1 [+ or -] 2.8 cd
25       Viability (%)     96.4                  98.1
         n                 (54)                  (53)
         Duration (days)   4.3 [+ or -] 2.2 b    4.2 [+ or -] 2.0 d
28       Viability (%)     79.1                  83.8
         n                 (68)                  (57)
         Duration (days)   5.5 [+ or -] 1.4 b    5.9 [+ or -] 1.6 cd
30       Viability (%)     81.6                  77.4
         n                 (31)                  (24)

T        Parameter         Instar
rees]C                     4th                   5th

         Duration (days)   --                    --
16       Viability (%)     0                     0
         n1                --                    --
         Duration (days)   12.2 [+ or -] 3.8 a   15.4 [+ or -] 2.3 a
19       Viability (%)     83.3                  95.0
         n                 (20)                  (19)
         Duration (days)   11.3 [+ or -] 3.7 a   14.0 [+ or -] 3.0 a
22       Viability (%)     89.6                  100.0
         n                 (26)                  (26)
         Duration (days)   5.7 [+ or -] 2.3 b    7.5 [+ or -] 2.5 b
25       Viability (%)     98.1                  98.1
         n                 (52)                  (51)
         Duration (days)   4.5 [+ or -] 2.4 b    5.5 [+ or -] 1.9 c
28       Viability (%)     96.5                  89.1
         n                 (55)                  (49)
         Duration (days)   5.7 [+ or -] 1.8 b    7.1 [+ or -] 2.5 bc
30       Viability (%)     83.3                  65
         n                 (20)                  (13)

T        Parameter         Development Cycle
rees]C                     (egg-adult)

         Duration (days)   --
16       Viability (%)     0
         n1                --
         Duration (days)   93.4 [+ or -] 17.0 a
19       Viability (%)     19.6
         n                 (19)
         Duration (days)   83.2 [+ or -] 17.7 b
22       Viability (%)     25.7
         n                 (26)
         Duration (days)   43.9 [+ or -] 8.6 c
25       Viability (%)     47.2
         n                 (51)
         Duration (days)   31.4 [+ or -] 5.9 d
28       Viability (%)     45.8
         n                 (49)
         Duration (days)   36.0 [+ or -] 6.5 cd
30       Viability (%)     11.1
         n                 (13)

(1) n = number of observations. * Means followed by the same letters
within a column are not significantly different at P<0.05 (Tukey

Table 2--Lower threshold temperature (Tl), thermal constant (K) in
degree-days, linear equation for the development velocity (1/D) and
coefficient of determination ([R.sup.2]) of the egg and nymph stages
(1st, 2nd, 3rd, 4th, and 5th instar), and total development
(egg-adult) of Neopamera bilobata fed unripe strawberry fruits of the
cultivar Aromas at 16, 19, 22, 25, 28, or 30 [+ or -] 1[degrees]C (70
[+ or -] 10% RH; 12h photophase).

Stage         Tl ([deg-   K       Regression Equation

Egg           13.1        121.8   1/D = -0.10758 + 0.00821 x
1st Instar    15.0        80.6    1/D = -0.18620 + 0.01240 x
2nd Instar    15.8        50.6    1/D = -0.31253 + 0.01976 x
3rd Instar    13.5        56.7    1/D = -0.23801 + 0.01765 x
4th Instar    14.2        57.4    1/D = -0.24647 + 0.01741 x
5th Instar    15.2        68.6    1/D = -0.22130 + 0.01457 x
Total         15.2        418.4   1/D = -0.03631 + 0.00239 x

Stage         [R.sup.2]   F          P

Egg           97.06       11715.16   <0.0001
1st Instar    95.35       1028.82    <0.0001
2nd Instar    69.92       115.97     <0.0001
3rd Instar    56.23       68.12      <0.0001
4th Instar    70.38       79.90      <0.0001
5th Instar    81.96       118.58     <0.0001
Total         88.24       433.12     <0.0001

Figure 2--Cumulative degree-days (DD) (A) and estimated number of
generations (B) of Neopamera bilobata per year in strawberry-
producing municipalities (1) in Brazil, based on mean annual
temperatures ([degrees]C) and annual cumulative degree-days (T1
value used was 15.19 and K of 418.41). Brazilian state
abbreviations: MG, Minas Gerais; PR, Parana; RS, Rio Grande do
Sul; SP, Sao Paulo. (1) For the municipalities of Sao Jose dos
Pinhais, Jaboti, Datas, and Pouso Alegre, data for Curitiba,
Joaquim Tavora, Diamantina, and Itajuba were used, respectively,
as they have similar climate conditions monitored by local
weather stations.


Estimated number of generations/year

City-State                 Estimated number of generations/year

Pouso Alegre--MG                4.3
Datas--MG                       2.9
Piedade--SP                     4.0
Atibaia--SP                     4.7
Sao Jose dos Pinhais--PR        2.0
Jaboti--PR                      5.1
Pelotas--RS                     2.9
Caxias do Sul--RS               1.9

Note: Table made from bar graph.
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Title Annotation:CROP PROTECTION; texto en ingles
Author:Kuhn, Taciana Melissa de Azevedo; Loeck, Alci Enimar; Botton, Marcos
Publication:Ciencia Rural
Date:Jan 1, 2018
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