Thermal effects on the biological parameters of bean Aphis craccivora (Hemiptera: Aphididae)

doi:10.21203/rs.3.rs-4960855/v1

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Thermal effects on the biological parameters of bean Aphis craccivora (Hemiptera: Aphididae)

https://doi.org/10.21203/rs.3.rs-4960855/v1

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The cowpea aphid Aphis craccivora is a polyphagous species that has spread worldwide. The aim of this study was to investigate the thermal effects on the developmental period, longevity, and fecundity of apterous females of A. craccivora. The experiment was conducted under the effects of four temperature regimes, which included 16°C, 20°C, 24°C, and 28°C, with 65 ± 5% relative humidity (RH) and a photoperiod of long-day 16:8 (L:D) h. Afterwards, the nymphs developed successfully until the adult stage at all temperature regimens. The developmental period of immature A. craccivora ranged from 10.6 days at 16°C to 5.0 days at 28°C. The nymph viability and survival were greater at 24°C than at the other temperatures. However, at a constant temperature of 28°C, the mortality rate was greater than that of the other species at the immature stage of A. craccivora. The lower developmental threshold for cowpea aphids was estimated at 1.77°C and 66.79 degree-days (DD) at the first instar until adulthood. The average longevity of adult females decreased from 22.2 days at 16°C to 10.8 days at 28°C. The net reproduction rate per female was 46.97 at 24°C and 26.93 to 28°C. The largest intrinsic rates of increase (r_m= 0.367) occurred at 28°C, and the smallest occurred at 16°C (r_m= 0.177). It was obvious that temperatures greater than 28°C resulted in good development, increased mortality at the nymphal stage, reduced adult longevity, and diminished fecundity. The optimal growth temperature for A. craccivora was 20°C-24°C.

Entomology

Behavioral Ecology

Developmental Biology

Population Biology

Adult longevity

life table

nymphal stage

nonlinear function

thermal resistance

Aphids (Hemiptera: Aphididae) are cosmopolitan and important pests in agroecosystems and are among the most devastating pests in tropical, subtropical, and temperate regions (Dedryver et al., 2010). From this family, the cowpea aphid Aphis craccivora represents one of the most crucial pests affecting the early stages of its host in Africa, Asia, and North America and causing intensive losses in horticultural crops as well as in forestry (Obeng-Ofori., 2007; Ou&edraogo et al., 2018). Parthenogenetic reproduction is the most disastrous damage caused by A. craccivora. The adult winged (alatae) plant causes less damage but is primarily responsible for the infestation of fields through its ability to fly from one place to another. Adults and nymphs feed on the undersurface of young leaves, stem tissues, growing tips, petioles, flowers, and fresh pods by piercing-sucking sap (Togola et al., 2017). Throughout the direct and indirect damage caused by A. craccivora, A. craccivora directly feeds by sucking sap and releasing honeydew, which creates fumagine (a sooty mold) on leaves, reducing the plant’s photosynthetic capacity. The bioactive substances injected through saliva interact with plant physiology, disturbing plant growth and development. Indirect damage is the result of virus transmission (Ebert & Cartwright, 1997; Blackman & Eastop, 2000). Plant damage is increasing because aphids, as virus hosts, are responsible for spreading viral diseases (Aldryhim & Khalil, 1993; Smith & Boyko, 2007). These include bean necrotic yellows virus, broad bean yellow mosaic virus, and bean leaf roll virus (Weigand & Bishara, 1991). The secretion of aphid honeydew reduces photosynthesis by releasing sooty mold on plant leaves (Klingler et al., 2001; Smith & Boyko, 2007).

Among the aforementioned types of aphid damage, abiotic and biotic factors play significant predominant roles in aphid biological life. In particular, abiotic factors affect aphids by modifying their life cycle. Aphids are ectothermic organisms, and abiotic factors strongly affect their development and growth until death. The reported data on the developmental rate and fecundity of cowpea aphids at several temperature regimens revealed different biological variations in Egypt (Hafiz., 2006), Riyadh, Kingdom of Saudi Arabia (Soffan & Aldawood, 2014), China (Zhaozhi et al., 2017), Korea (Cho et al., 2018), and Japon (MOUSA et al., 2019). The developmental and fecundity data for all aphid species, from one region to another, should be taken with considerable prudence for different crops because the aphid life table varies with alternating weather conditions. The findings on A. craccivora population parameters can be applied to developing IPM tactics, particularly in monitoring and simplifying the control methods of cowpea aphids in the Eastern Mediterranean region of Turkiye (Kersting et al., 1999; Satar et al., 2005). The aim of this work was to investigate the life-table parameters of the bean aphid A. craccivora on bean leaves at different temperature regimens under laboratory conditions.

Plant culture: Pinto bean (Phaseolus vulgaris L.) leaves were collected from the Department of Plant Protection Field Experimental in March 2020 at Adana, Saricam, Turkiye. After collection, the samples were transported to the laboratory and washed below flowing water for 5–10 minutes before use. Every five days, the old leaves were replaced with new leaves for better feeding by the individual insects.

Insect culture: Cowpea aphid adults (A. craccivora) were collected from Acacia trees in the Cukurova University area in Adana, Turkey. On average, 50 adults were reared inside 5 cages on common bean plants (F. vulgaris L.) at 24 ± 1°C and 65 ± 5% RH with a photoperiod of 16:8 h (L:D). The aphid fabae cages were established on fava bean plants and maintained for five generations prior to the start of the experiment to allow us to recover the net generation from maternal effects reflecting recent rearing conditions. The food A. craccivora was supplied daily to maintain the population stock (Fig. 1).

Experimental design

The experiment was conducted with randomly selected apterous females from stock cage culture and individually transferred to the undersurface of bean leaves on plastic Petri dishes (both 5 cm in diameter). For each temperature, a total of 4 replications of 10 Petri dishes per block with first-instar nymphs were placed inside an incubator. Forty Petri dishes were prepared with a wetted cotton pad (0.5 cm) and placed under the leaves such that the entire surface was covered to avoid drying. After that, 40 newborn aphids were carefully removed with a paintbrush from the master stock to the new Petri dishes. The moisture content of the cotton wool in the Petri dishes was maintained daily, and every 3–5 days, the aphids were transferred to new bean leaf discs. Freshly cultivated leaves were taken from the field and subsequently transported to the Citrus Entomology Laboratory at Cukurova University.

The experiments were conducted under four constant temperature regimes (16, 20, 24, and 28 ± 1°C) and 60 ± 5% relative humidity (RH) with a photoperiod of 16:8 (L:D) for 24 hours. For each temperature, the experiment started with 40 first-instar transferred nymphs. Every 24 h, nymphal development was recorded until the adult stage. After the adult period, the number of nymphs and survival of the mother aphids were recorded until the death of all adults of A. craccivora.

Statistical analysis

The developmental time and reproductive performance of A. craccivora were subjected to analysis of variance (ANOVA). The normality of the data was checked through the Shapiro–Wilk test. Differences in development time, longevity, and reproduction were calculated for each constant temperature. Multiple comparisons were tested using Tukey’s HSD multiple range test (P = 0.05) on significant variables. For each constant temperature, a curve was plotted with the Kaplan‒Meier product limit technique. Population growth rates were computed from the equation of Lotka (Birch, 1948) (Eq. 1).

1 = Σ e- * l* m (1)

where x = age in days (including immature stages), r = intrinsic rate of increase,

l_x= age-specific survival (including immature mortality), m_x = age-specific number of female offspring. After "r" was computed for the original data (r_all), differences among the r_m values were tested for significance differences by estimating variances through the jackknife method (Meyer et al., 1986). The jackknife pseudo value, r_j, was computed for the n samples using the following equation (Eq. 2):

r_j = n* r_all - (n-1) * r_i (2)

The means of the "n" jackknife pseudo values for each treatment were subjected to analysis of variance. Tukey’s HSD multiple range test was used to compare the mean growth rates at different temperature regimens (P < 0.05). Because low probability levels were used, there was no concern about inflation of experiment wise error rates (Jones, 1984). All of the abovementioned analyses were conducted using the Statgraphics software package version 11.5 (SPSS, Inc., Chicago, IL, USA) (Nie et al. 1975)

The development rates of the individuals reared at the different temperature levels were calculated via linear regression (y = a ± bx). The means (22°C) of the various temperatures at 16, 20, 24, and 28°C were used in the regression analysis. Afterward, the development threshold (-a/b) and thermal constant (the total effective temperature required to complete a generation, 1/b) of A. craccivora were estimated via linear regression (Campbel et al., 1974).

The development time of the cowpea aphid A. craccivora significantly decreased with increasing temperature, ranging from 5.0 days at 28°C to 10.6 days at 16°C (F = 81.786; fd = 3; P < 0.05) (Table 1). Linear regression analysis was applied to developmental points within the 16°C-28°C range. The temperature range increased linearly with increasing temperature (r _(T) = 0.015x – 0.0263; R² = 0.7959; F = 245.68; fd = 3; P < 0.05) (Fig. 1). The lower developmental threshold (LT) and thermal constant (K) of the A. craccivora nymphal stage were estimated to be 1.77°C, and 66.79 degree days (DD) were required for the first instar to become adults (Table 3). The longevity of the plants was significantly greater at 16°C (F = 17.858; fd = 3; P < 0.05) (Table 2). compared to any other temperature regime tested. The constant temperature for the highest number of offspring days occurred at 24°C (F = 2.74; fd = 3; P < 0.05) (Table 3). The highest average value of fecundity per reproductive day occurred at 24°C (F = 1.811; fd = 3; P < 0.05), and the lowest was at 16°C (Table 2).

Table 1

Development times (days ± SE) of *Aphis craccivora* on bean (*Phaseolus vulgaris*. L) at five constant temperatures, 65 ± 5% RH, and a photoperiod of 16:00 (L: D) h.
Temperature (°C)	n	I. Nymph period	II. Nymph period	III. Nymph period	IV. Nymph period	Total dev.
16°C	40	2.7 ± 0.14a	2.6 ± 0.16a	2.4 ± 0.31a	3.2 ± 0.28a	10.6 ± 0.42a
20°C	40	1.4 ± 0.08b	1.6 ± 0.12b	1.1 ± 0.10 c	1.7 ± 0.17b	6.0 ± 0.30b
24°C	40	1.0 ± 0.00c	1.1 ± 0.04c	1.8 ± 0.07ab	1.4 ± 0.10b	5.2 ± 0.16b
28°C	40	1.1 ± 0.05c	1.0 ± 0.06c	1.5 ± 0.12 bc	1.3 ± 0.12b	5.0 ± 0.17b
Significant differences between means (P < 0.05 and *P < 0.01) are expressed by different letters (a–b). The letters compare values in the same column.

Table 2

Preoviposition, oviposition, postoviposition, longevity, life span, and number of adult female *Aphis craccivora* individuals on bean (mean ± SE)
Temp (°C)	Pre-Oviposition (day)	Oviposition (day)	Post-Oviposition (day)	Longevity (day)	Life span (day)	Offspring (Aphid)
16	1.17 ± 0.2a	8.95 ± 1.5a	0.25 ± 0.1	22.2 ± 1.71a	11.6 ± 1.75a	32.1 ± 5.4
20	0.85 ± 0.1ab	6.77 ± 0.9ab	0.35 ± 0.4	14.1 ± 1.29b	8.1 ± 1.20ab	40.8 ± 6.2
24	0.45 ± 0.1b	6.32 ± 0.4ab	0.42 ± 0.1	12.4 ± 0.49b	7.2 ± 0.50b	45.2 ± 3.4
28	0.55 ± 0.1b	5.07 ± 0.8b	0.45 ± 0.1	10.8 ± 0.89b	5.8 ± 0.86b	26.9 ± 4.5
Significant differences between means (^P < 0.05 and ^*P < 0.01) are expressed by different letters (a–c). The letters compare values in the same column.

Table 3

Offspring/day, death ratio (%), wingless adults (n), wing adults (n), generation time (T0), net reproduction (Ro), and intrinsic rate of increase (rm) of *Aphis craccivora* on bean leaf discs at five temperature levels
Temp (°C)	N	Offspring reproductıon day(mean ± SE)	Death ratio (%)	Wingless adults(N)	Wing Adult(N)	(T₀)	(R₀)	(r_m)
16	40	3.6 ± 1.77	20	36	4	22.287	32.175	0.177
20	40	4.2 ± 0.47	20	40	3	13.294	40.850	0.321
24	40	6.5 ± 0.45	5	38	4	13.174	46.975	0.352
28	40	4.1 ± 0.45	28	35	5	10.191	26.925	0.367
Aphis craccivora (a) fourth nymphal stage, (b) aphid exoskeleton, skin or exuvia stage, (c) adult stage, and (d) first nymphal stage.

The highest % mortality rate was observed at 28°C, possibly because of the vulnerability to high temperature at the first nymphal stage (Table 3). The survival rate of A. craccivora adults sharply diminished after the peak of nymph production at higher temperatures. More wingless adults were observed at 20°C. However, at 28°C, there were more winged or alate plants (Table 3). According to the biological development of aphid species at warm temperatures, the possibility of developing winged individuals is greater. At 16°C and 20°C, the post oviposition period was relatively long compared to that at the other temperatures. (Fig. 3) (Table 2). The number of reproductive offspring per period of day varied between 3.6 days (16°C) and 6.5 days (24°C) (Table 3). Augmenting the temperature resulted in shorter generation times (T_o) of A. craccivora, with 22.3 days at 16°C and 10.2 at 28°C (Table 3). The net reproduction rate (R_o) was highest at 24°C (64.97 aphids/aphid) and lowest at 28°C (26.93 aphids/aphid) (Table 3). A greater population of A. craccivora resulted in a greater per capita rate of population growth, as indicated by the intrinsic rate of increase at 28°C (0.367 aphids/aphid per day) compared to that at 16°C (0.177 aphids/aphid) (Table 3).

The developmental rate (r) of A. craccivora at four constant temperatures, all of which were alternated (variation cycle), was fitted with a linear regression equation, and the developmental rate ranged between 16°C and 28°C (Table 4). The mean alternating temperatures were used to fit the linear regression equation. The development time of A. craccivora increased linearly with increasing temperature. The development rates of A. craccivora at four temperature regimens were fitted to the linear regression equation y = a ± bx (Table 4). The outcomes of the regression model were fitted separately for the data obtained from female A. craccivora at the developmental rate. The equation for female development was calculated as follows: Y = 0.015 × -0.0263 (R2 = 0.97; P ≤ 0.05) from the first instar to the developmental stage and adult stage (Fig. 2): through these equations, the development thresholds and thermal constants were calculated.

Table 4

Regression equations and parameters of development period rates of *Aphis craccivora* on bean leaves under different constant temperatures
Parameters	Nymph I	Nymph II	Nymph III	Nymph IV	Adult
Equation of regression	y = -0.13x + 4.4 R² =0.730	y= -0.13x + 4.49 R² = 0.873	y = -0.05x + 2.8 R² = 0.222	y = -0.15x + 5.2 R² = 0.769	y = -0.44x + 16.38 R² = 0.743
Thermal constant (1/a) (°C day)	7.69	7.54	20	6.67	2.27
Development threshold (b/a) (°C)	260.08	225.50	1120	231.22	84.51

Table 5

ANOVA of several biological parameters of *Aphis craccivora* at five temperature regimens on the bean. A P value less than 0.05 indicated that there were significant differences between parameters in this study. As we can see only for offspring per day, postoviposition, and lifespan, there was no significant difference because the p value was > 0.05.
Biological parameters	Between Groups	Sum of Squares	df	Mean Square	F	Sig.
Lifespan		726.069	3	242.023	4.340	0.006‘**’
Offspring		8192.725	3	2730.908	2.744	0.045 ʿ*ʾ
Longevity		3043.850	3	1014.617	17.858	0.000***
N1		79.269	3	26.423	80.311	0.000***
N2		69.525	3	23.175	44.938	0.000***
N3		35.469	3	11.823	9.221	0.000***
N4		93.869	3	31.290	22.590	0.000***
Total-development		824.269	3	274.756	81.786	0.000***
Preoviposition		12.819	3	4.273	5.024	0.002‘**’
Oviposition		312.919	3	104.306	2.519	0.060‘*’
Postoviposition		85.119	3	28.373	10.715	0.000***
Offspring/day		205.626	3	68.542	1.811	0.147‘.’

In the ecosystem, insects are not subjected to constant or alternating temperatures. However, laboratory conditions can provide valuable insight into the population dynamics of aphids. The findings reported here clearly show the effects of temperature on the development time, death rate, longevity, and fecundity of A. craccivora. Aphid species are small ectothermic insects that are strongly related to temperature. Recall that temperature influences multiple aspects of insect biology, such as the metabolic system and developmental rate, as well as the timing and level of insect activities. Temperatures beyond the thresholds of development for a given insect can slow growth, and extreme temperatures can kill members of the insect population. It is logical that temperature fluctuations can cause changes in insect biology. In this study, we have discussed how temperature alternations affect insect biology. Several biological parameters of Aphis craccivora were also evaluated. The maximum temperature for the development of A. craccivora was 28°C (mean = 5.0 days; F = 81.78; P = 0.05), but other studies have reported a temperature of 30°C (Cho et al., 2018; Kuo, M. H. & Chen, 2004) and a temperature of 29.4°C (Berberet et al., 2009; Girão et al., 2019) on bean plants. These results correlate with the degree to which ectothermic animals that develop under warm conditions tend to grow faster and mature earlier. On the other hand, these animals are slower in maturation than are similar animals that develop under cool conditions. The preoviposition period, during which the temperature is held constant and gradually decreases, delays the occurrence of fecundity. The temperature increases from 16°C to 24°C, similar to the 16°C and 25°C reported by (Cho et al., 2018; Girão et al., 2019). The number of oviposition days strongly depends on the area in which the insect is evaluated by using food and weather resources. Normally, at both low- and high-tolerance temperatures, insects can take a long time to reproduce, for example, from 16°C to 28°C (mean = 8.95, 5.07; F = 2.519; P = 0.05). The same tendency at 15, 20, and 25°C was reported by (Cho and et al., 2018) and at 18, 22, 25, and 28°C. (Girão et al., 2019).

The postoviposition period was 16°C (mean day = 2.05; F = 2.519; P = 0.05) if it was below the lowest relative temperature for good reproduction; during this time, the duration after the offspring period became longer than the adaptive temperatures reported at 18, 22, 25, and 28°C (Girão, et al., 2019) (mean days = 1.2, 0.8, 0.8, and 0.2, respectively). Longevity increases inversely with decreasing temperature, as we can see at 16°C (22.2 days) and 28°C (10.8 days); however, in the literature, approximately the same constant temperatures were reported at 18°C and 28°C by (Girão et al., 2019).

However, there were differences between the results presented in this research within the life span of A. craccivora. The temperature regimes exhibited significant differences from the highest to lowest temperature at 28°C and 16°C (mean/day) (5.8 and 11.6, F = 4.340; P = 0.05, respectively). The mean values between the life span temperatures were similar: at 28°C, the lowest occurred at 16°C, and the highest occurred at 28°C. These findings revealed that there were no significant differences. These results indicate that these temperatures are amenable to survival for aphid species. (Table 2). In general, these observations established the inverse proportional relationship between oviposition periods and immature stages produced per female per day in the temperature range of 16 to 28°C, in contrast to the results presented by(Berberet et al., 2009; Girão et al., 2019).

According to these results, there are many possible adaptations between several studied aphid populations. For example, the variations observed in thermal constant development based on the suitable temperature for black aphids on the bean might be explained in part by the functional theory of life, which relates to the highest value for a development threshold and the smallest value for total thermal requirement, as expected, for species more adapted to tropical regions and temperate regions (Trudgill & Perry, 1994; Brown et al., 1995).

Conflict of interest The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Acknowledgments We would like to thank the team management of the Project Development and Coordination Unit. This research was part of the Master’s degree thesis of Rochelyn DONA and was funded by the Project Development and Coordination Unit of Cukurova University (Grant Code: FYL-2020-12688).

Funding This study was supported by Cukurova University. (Grants Code: FYL-2020-12688).

Authors ‘contributions RD and SS conceived, designed and performed research. Both of the authors analyzed data, and wrote the manuscript. Both authors read and aprouved the manuscript.

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The authors declare no competing interests.

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Thermal effects on the biological parameters of bean Aphis craccivora (Hemiptera: Aphididae)

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