Aphis gossypii Glover and Acyrthosiphon gossypii Mordvilko (Hemiptera: Aphididae) are important pests of cotton (Gossypium hirsutum L.) in Xinjiang, China, that reduce yield and lint quality. We studied competition between the two aphid species in laboratory arenas to better understand population change and competitive advantage between the two and to provide a theoretical basis for the observed population outbreak of aphids in cotton fields. To study intraspecific competition, densities of 5, 10, and 15 aphids per 5-cm-diameter leaf disc were established in individual 6-cm-diameter arenas. Equal numbers of each species were placed on leaf discs in the arenas to establish densities of 3, 5, and 10 aphids of each species per leaf disc to assess interspecific competition. In intraspecific competition assays, the mean generation time (T) and the net reproductive rate (Ro) of both species decreased as aphid density increased, while the intrinsic rate of increase (r) and finite rate of increase (λ) of Acy. gossypii increased as density increased. In interspecific competition assays, population growth of A. gossypii was higher than with Acy. gossypii at the same density, while the mean generation time of A. gossypii was less than with Acy. gossypii. The net reproductive rate, intrinsic rate of increase, and finite rate of increase were higher in A. gossypii than in Acy. gossypii. Density is a key factor affecting competition between A. gossypii and Acy. gossypii. The higher the density, the more intense the interspecific competition, with interspecific competitiveness of A. gossypii stronger than that of Acy. gossypii.

Due to food and space constraints, insects have competitive, reciprocal, partial, or neutral relationships (Denno et al. 1995). In these relationships, competition is an important factor affecting community structure (Iwabuchi and Urabe 2012; Soares 2013; Utsumi et al. 2010). This competition may occur between individuals of the same species, e.g., intraspecific competition, or between individuals of different species, e.g., interspecific competition (Barabas et al. 2016; Reitzl and Trumble 2002; Zhao et al. 2017). Multiple factors influence interspecific and intraspecific competitive relationships during competition in insect populations (Duan et al. 2016; Gergs et al. 2013; Jordan and Tomberlin 2017). Generally, external factors such as temperature, humidity, light, precipitation, and pesticides are considered to have an important impact on insect competition (Marchioro and Foerster 2011, 2016; Mohammed et al. 2019; Qu et al. 2020; Savopoulou-Soultani et al. 2012). However, the key role of density-dependent effects in population regulation in competition cannot be ignored (Li and Akimoto 2021; Magneville et al. 2018). Density directly affects population growth rate, development duration, life span, and offspring production, and ultimately affects population quantity change (Naselli et al. 2017; van Veen et al. 2006).

Intraspecific and interspecific density-dependent effects are common in most herbivorous insects, especially in Hemiptera and Homoptera with piercing-sucking mouthparts (Denno and Roderick 1992). Density-dependent effects directly affect population life parameters in the competitive relationships of aphids, such as Acyrthosiphon pisum (Harris), Myzus persicae (Sulzer), and Lipaphis erysimi (Kaltenbach), and the planthoppers such as Nilaparvata lugens (Stal), Sogatella furcifera (Horváth), and Laodelphax striatellus (Fallén) (Hu et al. 2004; Li and Akimoto 2021; Lü et al. 2011; Zhao et al. 2001). For these insects with similar ecological habits and niches, the constraint of density effect in competition will be more prominent (Chongrattanameteekul et al. 1991; Gonzalez-Megias and Gomez 2003). These insects consume available resources in limited space and increase intraspecific and interspecific competition (Klepsatel et al. 2018; Reis et al. 1999; Villemereuil and Lopez-Sepulcre 2011). As individuals with insufficient resources die, population density decreases with heightened risk of population collapse (Karban 1986; Thirakhupt and Araya 1992). At the same time, population growth strategies of individuals may adjust to compensate. These include development period, body weight, life span, and others (Morimoto et al. 2019; Than et al. 2020; Tsurim et al. 2018). Therefore, the density effect not only restricts population size (Mueller et al. 1991) but also affects individual growth and reproduction (Diamantidis et al. 2020; Henry et al. 2018; Kaplan and Denno 2007; Morimoto et al. 2016,).

The primary aphid pests of cotton (Gossypium hirusutum L.) grown in Xinjiang, China, are Aphis gossypii Glover and Acyrthosiphon gossypii Mordvilko (Hemiptera: Aphididae). Feeding by both species causes leaf curling, delays budding and flowering, causes abscission of buds and bolls, and reduces cotton yield and quality (Gao et al. 2013; Hullé et al. 2020; Moran and Whitham 1990). Aphis gossypii and Acy. gossypii can occur at the same time in cotton fields, but the two have different temporal characteristics (Lü et al. 2002; Yao 2017). In normal years, the temperature is relatively low before and after cotton seedling emergence to the budding period when Acy. gossypii is the dominant species of the two; A. gossypii is the dominant species in the middle and late stages of cotton growth (Gao et al. 2012; Li et al. 2008; Yao 2017). Aphis gossypii and Acy. gossypii have similar niche and living habits in cotton, so there is a strong competitive relationship in the dynamic changes of population structure (Gao et al. 2013; Lü et al. 2002). Previously, interspecific and intraspecific competition between A. gossypii and Acy. gossypii were studied in response to temperature, natural enemies, cotton–host-plant resistance, pesticide stress, and other external factors (Feng et al. 2015; Gao et al. 2012; Yao 2017). In our previous study, we confirmed that the feeding behavior of A. gossypii and Acy. gossypii also was an important factor in mediating the competition between the two species (Deng et al. 2013; Wu et al. 2020; Yan et al. 2019, 2020; Zhang et al. 2020). These studies have helped us to better understand the competition between the two species. However, no study has yet investigated the intraspecific and interspecific competition in response to density of A. gossypii and Acy. gossypii.

Therefore, in this study, A. gossypii, Acy. gossypii, and their mixed populations were established at different densities in laboratory arenas. The effects of density on the growth and development, population number, and life parameters of A. gossypii and Acy. gossypii were thus observed and calculated to clarify intraspecific competition and interspecific competition in response to density.

Insects. Colonies of A. gossypii and Acy. gossypii were initially established from aphids collected from cotton fields growing in Shihezi University fields. Over 30 generations of each species had been maintained in the laboratory on cotton in an environmentally controlled chamber at 26 ± 1°C, 70 ± 5% relative humidity, and a photoperiod of 16 h:8 h (L:D).

Assay arenas. Five-centimeter-diameter circular discs were cut from newly emerged cotton leaves that had been excised from the plant, washed, and air dried. The discs were inverted with abaxial surface facing up and placed onto 1% agar gel that had been previously poured and allowed to cool in 6-cm-diameter Petri dishes.

Assay design. We used the leaf disc method to measure population production time, duration, quantity, and life span in response to intraspecific and interspecific competition. For intraspecific competition, aphid nymphs obtained from the respective laboratory colonies were placed individually on leaf discs to a total of 5, 10, and 15 aphids per disc for each species. The arenas were covered, and the aphids were observed for 20 d. We observed and recorded aphids on leaf discs at 8:00 a.m. and 8:00 p.m. each day. In recording the immature stages of aphids, we determined the age of aphids according to the number of molts, and the molted exuviae were removed after each observation. The period from the molting of fourth instar nymphs to appearance of adult aphids was recorded at the prereproductive period. We recorded the daily aphid production, survival number, and population number. The three treatments for each species were replicated 10 times with one arena representing a replicate.

Interspecific competition responses were measured by placing both A. gossypii and Acy. gossypii nymphs on individual leaf discs. The treatments were (a) 3 A. gossypii and 3 Acy. gossypii nymphs per disc; (b) 5 A. gossypii and 5 Acy. gossypii nymphs per disc, and (c) 10 A. gossypii and 10 Acy. gossypii nymphs per disc. We observed and recorded aphids on leaf discs at 8:00 a.m. and 8:00 p.m. each day. We recorded the molting of aphids, daily aphid production, survival number, and population number. Each treatment was replicated 10 times with one arena representing a replicate. Nymphs were obtained from the respective laboratory colonies and observed for 15 d.

Calculations and analyses. Using the age-stage, two-sex life table theory (Chi 1988; Chi and Liu 1985), the data recorded from the various treatments were used to calculate developmental duration of nymphs plus prereproductive adults. The age-specific survival rate (lx) and age-specific fecundity (mx) were calculated according to the survival of aphids at different developmental stages and the nymph production by females as recorded daily. Net reproductive rate (R0), or the total number of offspring produced by an individual, was then calculated by the formula,

formula

An R0 value of 1.0 indicates that a population is neither increasing nor decreasing. Likewise, the intrinsic rate of increase (r) was estimated by the Euler–Lotka formula,

formula

and provides an estimate of continuous population growth when environmental resources are hypothetically unlimited. The finite rate of increase of the population (λ) was calculated as λ = er, which indicates population increase over time, with λ = 1 being a stable population. The mean generation period (T) refers to the time required to increase R0 when the population reaches a stable age-stage distribution and a stable growth rate, namely erT=R0 or λT =R0. The formula for calculating T was T = ln R0/r.

Calculations were conducted using the program TWOSEX-MSChart (Chi 2022). The least significant differences (LSD) multiple comparison method of the statistical software SPSS (Statistical Package for the Social Sciences, Version 18.0, Chicago, IL) was used to identify treatment differences in developmental duration. The mean values of life table parameters were estimated using the bootstrap method of Akkopru et al. (2015), and LSD was used to separate treatment means.

Acyrthosiphon gossypii density-dependent response to intraspecific competition. The population growth curves (Fig. 1) of Acy. gossypii at the three aphid densities were similar in shape and appearance. During the 20 d of observation, the numbers of aphids remained constant initially, then increased to respective peaks and quickly declined. As might be expected, we observed differences in the timing of these phases of the curve with respect to initial aphid density. Numbers of aphids increased and peaked earlier in the observation period in the initial 15 aphids/disc than in the treatments with 10 and 5 aphids/disc.

Fig. 1

Population growth of Acyrthosiphon gossypii in response to densities of 5, 10, and 15 aphids per 5-cm leaf disc.

Fig. 1

Population growth of Acyrthosiphon gossypii in response to densities of 5, 10, and 15 aphids per 5-cm leaf disc.

Close modal

We found no significant influence on the duration of the individual nymphal stages in response to initial aphid density, but mean (±standard deviation) duration of the prereproductive period in the treatment of 5 aphids/disc (2.85 ± 0.88 d) was significantly longer than either the 15 (1.30 ± 0.80 d) or 10 (1.75 ± 0.72 d) aphids/disc treatments (F = 21.59; df = 2, 279; P < 0.0001; Table 1). With respect to the life table parameters, the mean generation time (T) was longer in the treatment with 5 aphids/disc than in the other two treatments, while the intrinsic rate of increase (r) was significantly lower than either the 15 or 10 aphids/disc treatment (F = 131.28; df = 2, 29; P < 0.0001; Table 2). We found no significant differences in the net reproductive rate (R0) or the finite rate of increase (λ) among the density treatments for Acy. gossypii (P > 0.05; Table 2). The population doubling time was significantly higher in the treatment with 10 aphids/disc (12.41 ± 1.23 d) than in either the 15 aphids/disc (2.85 ± 1.08 d) or the 5 aphids/disc (3.76 ± 0.91 d) treatments (F = 67.29; df = 2, 29; P < 0.0001; Table 2).

Table 1

Duration in days (mean ± standard deviation) of immature stages of development of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*

Duration in days (mean ± standard deviation) of immature stages of development of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*
Duration in days (mean ± standard deviation) of immature stages of development of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*
Table 2

Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*

Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*
Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to intraspecific competition at three densities of aphids per 5-cm leaf disc.*

Aphis gossypii density-dependent response to intraspecific competition. The population growth curves for the A. gossypii density treatments were similar to those of A. gossypii (Fig. 2). In the treatment with 15 aphids/disc, the increase in aphid numbers occurred earlier in the observation period than the treatments with 10 and 5 aphids/disc. The 20-d observation period was not sufficiently long to note population collapse in any of the treatments. The duration of the immature stages of A, gossypii did not differ among the density treatments (P > 0.05; Table 1).

Fig. 2

Population growth of Aphis gossypii in response to densities of 5, 10, and 15 aphids per 5-cm leaf disc.

Fig. 2

Population growth of Aphis gossypii in response to densities of 5, 10, and 15 aphids per 5-cm leaf disc.

Close modal

Of the life table parameters, mean generation time (T) and net reproductive rate (R0) were not significantly affected by aphid density (P > 0.05; Table 2). The intrinsic growth rate (r) was significantly lower in the treatment with 15 aphids/disc in comparison to the treatments with either 10 or 5 aphids/disc (F = 35.70; df = 2, 29; P = 0.0016; Table 2), while the finite rate of increase (λ) when compared among treatments was highest in the treatment with 10 aphids/disc (F = 114.59; df = 2, 29; P < 0.0001; Table 2). As with Acy. gossypii, the doubling time of A. gossypii was significantly longer in the 10 aphids/disc treatment (10.02 ± 1.35 d) in comparison to either the 5 (2.28 ± 0.53 d) or 15 (2.18 ± 0.97 d) aphids/disc treatments (F = 45.17; df = 2, 29; P < 0.0001; Table 2).

Acyrthosiphon gossypii and A. gossypii responses to mixed population density. When aphids of both species were placed on the same leaf disc, the numbers of A. gossypii increased to higher levels than did Acy. gossypii, regardless of the initial density of the mixed population (Fig. 3). For example, in the arenas with an initial density of three A. gossypii and three Acy. gossypii aphids per disc, the numbers of A. gossypii increased 13-fold, while the numbers of Acy. gossypii increased 4.3-fold (Fig. 3A). Likewise, in the treatment with five aphids of each species per leaf disc, the numbers of A. gossypii increased 18.8-fold at peak numbers, while Acy. gossypii numbers increased only 5.6-fold before declining after the 10th day (Fig. 3B). Increases were 5.6-fold in A. gossypii numbers and 2.7-fold in Acy. gossypii numbers in the treatment with 10 aphids of each species per leaf disc (Fig. 3C).

Fig. 3

Population growth of Acyrthosiphon gossypii and Aphis gossypii in response to combined densities of 3 (A), 5 (B), and 10 (C) aphids of each species per 5-cm leaf disc.

Fig. 3

Population growth of Acyrthosiphon gossypii and Aphis gossypii in response to combined densities of 3 (A), 5 (B), and 10 (C) aphids of each species per 5-cm leaf disc.

Close modal

We also compared responses in duration of developmental stages and life table parameters to the three mixed population densities within each species. There were no significant differences (P > 0.05) in the duration of the four nymphal stages of Acy. gossypii among the mixed population densities, but the duration of the prereproductive period in the lowest density (three aphids of each species) was significantly longer than in the other two density levels (F = 31.32; df = 2, 157; P < 0.0001; Table 3). No significant differences (P > 0.05) were detected in the duration of the first, second, and third instars of A. gossypii among the density treatments, but the duration of the fourth instar (F = 14.50; df = 2, 170; P < 0.0001) and the prereproductive period (F = 9.49; df = 2, 165; P = 0.0008) were significantly longer in the lowest density treatment than in the higher two densities (Table 3).

Table 3

Duration in days (mean ± standard deviation) of immature stages of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

Duration in days (mean ± standard deviation) of immature stages of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*
Duration in days (mean ± standard deviation) of immature stages of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

For Acy. gossypii, the mean generation time (T) was significantly longer (F = 12.51; df = 2, 29; P = 0.0037) and the intrinsic rate of increase (r) was significantly lower (F = 49.36; df = 2, 29; P < 0.0001) in the lowest density (3 aphids of each species) of the mixed population treatment than in either of the other density treatments (5 aphids of each species and 10 aphids of each species (Table 4). In comparing the three density treatments, the net reproductive rate (R0) was significantly lower in the treatment of five aphids of each species in the mixed population than in other treatments (F = 5.56; df = 2, 29; P = 0.0095; Table 4). There were no significant differences among the treatments in finite rate of increase (λ) and doubling time (P > 0.05; Table 4).

Table 4

Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*
Estimated (mean ± standard deviation) life parameters of Acyrthosiphon gossypii and Aphis gossypii in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

With A. gossypii, no significant differences were detected in mean generation time (T) or doubling time (P > 0.05; Table 4). The net reproductive rate (R0) (F = 16.73; df = 2, 29; P < 0.0001), intrinsic rate of increase (r) (F = 43.33; df = 2, 29; P = 0.0021), and finite rate of increase (λ) (F = 34.31; df = 2, 29; P < 0.0001) in the highest density treatment were significantly lower than those of the other two density treatments (Table 4).

In comparing each of the immature stages calculated for the two species in mixed populations, there were no significant differences in the duration of the first instar stage in the lowest density (3 aphids of each species) and prereproductive period in the treatment of 5 aphids of each species (P > 0.05), second (3 aphids of each species: F = 21.88; df = 1, 56; P = 0.0097; 5 aphids of each species: F = 13.49; df = 1, 97; P = 0.0043; 10 aphids of each species: F = 8.36; df = 1, 195; P = 0.0012), third (3 aphids of each species: F = 10.20; df = 1, 54; P = 0.0050; 5 aphids of each species: F = 38.05; df = 1, 92; P < 0.0001; 10 aphids of each species: F = 35.41; df = 1, 193; P = 0.0087), and fourth stages (3 aphids of each species: F = 30.43; df = 1, 54; P < 0.0001; however, 5 aphids of each species: F = 116.00; df = 1, 92; P < 0.0001; 10 aphids of each species: F = 32.26; df = 1, 187; P < 0.0001) were significantly shorter for A. gossypii than Acy. gossypii at each of the aphid densities (Table 5).

Table 5

Comparison of Acyrthosiphon gossypii and Aphis gossypii immature stages (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

Comparison of Acyrthosiphon gossypii and Aphis gossypii immature stages (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*
Comparison of Acyrthosiphon gossypii and Aphis gossypii immature stages (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

In comparing each of the life table parameters calculated for the two species in mixed populations, we found that the mean generation time (T) (3 aphids of each species: F = 12.96; df = 1, 19; P < 0.0001; 5 aphids of each species: F = 61.19; df = 1, 19; P < 0.0001; 10 aphids of each species: F = 60.15; df = 1, 19; P < 0.0001), and the generation doubling time (3 aphids of each species: F = 37.64; df = 1, 19; P < 0.0001; 5 aphids of each species: F = 20.86; df = 1, 19; P < 0.0001; 10 aphids of each species: F = 6.39; df = 1, 19; P = 0.0211) were significantly shorter for A. gossypii than for Acy. gossypii at each of the aphid densities (Table 6). Furthermore, the net reproductive rate (R0) (3 aphids of each species: F = 32.08; df = 1, 19; P < 0.0001; 5 aphids of each species: F = 45.95; df = 1, 19; P < 0.0001; 10 aphids of each species: F = 7.60; df = 1, 19; P = 0.0130), intrinsic rate of increase (r) (3 aphids of each species: F = 15.22; df = 1, 19; P = 0.0011; 5 aphids of each species: F = 9.43; df = 1, 19; P < 0.0001; 10 aphids of each species: F = 29.33; df = 1, 19; P < 0.0001), and finite rate of increase (λ) (3 aphids of each species: F = 25.17; df = 1, 19; P < 0.0001; 5 aphids of each species: F = 63.70; df = 1, 19; P = 0.0022; 10 aphids of each species: F = 7.09; df = 1, 19; P = 0.0003) of A. gossypii were significantly lower than with Acy. gossypii at all aphid densities (Table 6).

Table 6

Comparison of Acyrthosiphon gossypii and Aphis gossypii life parameters (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

Comparison of Acyrthosiphon gossypii and Aphis gossypii life parameters (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*
Comparison of Acyrthosiphon gossypii and Aphis gossypii life parameters (mean ± standard deviation) in response to interspecific competition at three densities of mixed populations of aphids per 5-cm leaf disc.*

Intraspecific density effects are common in herbivorous insects, but there are some differences in strength of response (Chongrattanameteekul et al. 1991). As numbers increase to a point of limiting resources, the population will reach an equilibrium or experience a decline in numbers, or both (Karban 1986; Thirakhupt and Araya 1992). Our results with single populations of A. gossypii and Acy. gossypii (i.e., intraspecific competition) well illustrated these observations and results. At initial densities of 5, 10, and 15 aphids per 5-cm leaf disc, numbers of aphids initially remained relatively constant for several days, then increased exponentially until reaching a level at which undefined density-dependent factors limited population growth, resulting in a rapid decline in numbers (Figs. 1, 2). Regardless of our initial treatment densities, the numbers of A. gossypii increased to higher levels than Acy. gossypii in these tests, thus indicating that the threshold for tolerance of population growth limiting factors is greater for A. gossypii than for Acy. gossypii.

When the insect population density reaches or exceeds this threshold, limiting factors associated with density can reduce survival rate, change sex ratio, reduce fertility and resistance to disease, and induce diapause, dormancy, and developmental deformity, thus affecting population growth (Xu 1987). For example, the larval density of the leafminers Liriomyza trifolii (Burgess) and Liriomyza sativae Blanchard significantly affects survival rate, mean pupal weight, pupation rate, emergence rate, adult longevity, and fecundity per female (Yi et al. 2014). In our study, the mean generation time (T) of Acy. gossypii significantly decreased with increased aphid density, while the intrinsic rate of increase (r) value increased with higher density levels (Table 2). Of the aphid densities tested, the intermediate density of 10 aphids/leaf disc had a significantly longer population doubling time than did the 5 and 15 aphids/leaf disc densities. We saw a similar response in doubling time for A. gossypii at the intermediate density in comparison to the low and high densities tested (Table 2). Other significant differences among the density treatments were recorded with intrinsic rate of increase (r) (e.g., high density level significantly higher) and finite rate of increase (λ) (e.g., intermediate density level significantly higher).

Inherent competitiveness of insects varies among species. In interspecific interactions, the species with strong competitive advantages can exploit niche factors to displace the weaker species, as reported for Bemisia tabaci (Gennadius) biotypes (Pan et al. 2010) and Liriomyza spp. (Yi et al. 2014). This phenomenon is also evident in interspecific competition among herbivorous insects such as thrips (Wang et al. 2011), mites (Yan et al. 2010), and whiteflies (Zheng et al. 2012).

Our results appear to corroborate those results when A. gossypii and Acy. gossypii aphids are in a mixed populations for 15 d. As previously noted, when A. gossypii and Acy. gossypii aphids were placed on the same leaf disc, the numbers of A. gossypii increased to higher levels than did Acy. gossypii, regardless of the initial density of the mixed populations (Fig. 3). The ecological equilibrium of A. gossypii in our test arenas is higher than that of Acy. gossypii, which might be attributed to differences in life parameters, differences in tolerance of undefined limiting factors, differences in capabilities to exploit the ecological niche created in the arena, or any combination of those factors. Furthermore, we postulate that these factors operate in Chinese cotton fields where A. gossypii tends to become the dominant aphid species as the growing season progresses. Our life parameters data show that A. gossypii possesses several characteristics that contribute to its competitive success over Acy. gossypii. Regardless of aphid density, the mean generation time (T) of A. gossypii was significantly shorter than that of Acy. gossypii, and the net reproductive rate (R0), intrinsic rate of increase (r), and finite rate of increase (λ) of A. gossypii were significantly lower than for Acy. gossypii (Table 6). These contributed to the significantly lower population doubling time of A. gossypii than of Acy. gossypii.

When challenged by abiotic or biotic limiting factors (e.g., temperature, pesticides, host plant resistance, population density, food availability) (Feng et al. 2015; Gao et al. 2012; Meng and Li 2000; Yao 2017), A. gossypii adapts more readily than does Acy. gossypii. This is at least one explanation of how A. gossypii becomes the dominant aphid species when A. gossypii and Acy gossypii occupy the same cotton plants in production fields. We also postulate that this observed competitive advantage evolved through interspecific competition for the same resources.

Admittedly, the design of this study in closed arenas had some limitations, especially with regard to movement of aphids to and from host plants that commonly occurs in natural environments. However, analyses using the age-stage, two-sex life table effectively reflected the intraspecific and interspecific competition dynamics of Acy. gossypii and A. gossypii. Future studies should be designed and conducted in larger spaces to better simulate field conditions.

The raw data from this study that support the conclusions of this paper will be made available by the authors upon request, without undue reservation.

This research was supported by the National Natural Science Foundation of China (Grant No. 31660519).

Akkopru,
E.-P.,
Atlihan
R.,
Okut
H.,
and
Chi
H.
2015
.
Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars.
J. Econ. Entomol.
108
:
378
387
.
Barabas,
G.,
Michalska-Smith
M.J.
and
Allesina
S.
2016
.
The effect of intra- and interspecific competition on coexistence in multispecies communities.
Am. Nat.
188
:
E1
E12
.
Chi,
H.
1988
.
Life-table analysis incorporating both sexes and variable development rates among individuals.
Environ. Entomol.
17
:
26
34
.
Chi,
H.
2022
.
TWOSEX-MSChart: Computer program for age stage, two-sex life table analysis.
National Chung Hsing University
,
Taichung, Taiwan
.
4 September 2019.
( ).
Chi,
H.
and
Liu
H.
1985
.
Two new methods for the study of insect population ecology.
Bull. Inst. Zool. Acad. Sinica
24
:
225
240
.
Chongrattanameteekul,
W.,
Foster
J.E.
and
Araya
J.E.
1991
.
Biological interactions between the cereal aphids Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Hom., Aphididae) on wheat.
J. Appl. Entomol.
111
:
249
253
.
Deng,
X.-X.,
Jiang
H.-L.,
Peng
J.,
He
Z.-M.,
Ma
T.-W.
and
Wang
J.-G.
2013
.
Physiological responses of cotton to feeding by Aphis gossypii during the flower-bolling stage.
Chinese J. Appl. Entomol.
50
:
161
166
.
Denno,
R.F.,
Mark
S.
and
McClure
M.S.
1995
.
Interspecific interactions in phytophagous insects: Competition reexamined and resurrected.
Annu. Rev. Entomol.
40
:
297
331
.
Denno,
R.F.
and
Roderick
G.K.
1992
.
Density-related dispersal in planthoppers: Effects of interspecific crowding.
Ecology
73
:
1323
1334
.
Diamantidis,
A.D.,
Ioannou
C.S.,
Nakas
C.T.,
Carey
J.R.
and
Papadopoulos
N.T.
2020
.
Differential response to larval crowding of a long- and a short-lived Medfly biotype.
J. Evol. Biol.
33
:
329
341
.
Duan,
M.,
Liu
Y.,
Yu
Z.,
Baudry
J.,
Li
L.,
Wang
C.
and
Axmacher
J.C.
2016
.
Disentangling effects of abiotic factors and biotic interactions on cross-taxon congruence in species turnover patterns of plants, moths and beetles.
Sci. Rep.
6
:
23511
.
Feng,
L.-K.,
Gao
G.-Z.,
Lv
Z.-Z.,
Jia
H.-M.
and
Wang
P.-L.
2015
.
Interspecific competition between Aphis gossypii Glover and Acyrthosiphon gossypii Mordviiko at different temperatures.
Chinese J. Appl. Entomol.
52
:
557
565
.
Gao,
G.-Z.,
Z.-Z.,
Sun
P
and
Xia
D.-P.
2012
.
Effects of high temperature on the mortality and fecundity of two co-existing cotton aphid species Aphis gossypii Glover and Acyrthosiphon gossypii Mordvilko.
Chinese J. Appl. Ecol.
23
:
506
510
.
Gao,
G.-Z.,
Perkins
L.E.,
Zalucki
M.P.,
Z.-Z.
and
Ma
J.-H.
2013
.
Effect of temperature on the biology of Acyrthosiphon gossypii Mordvilko (Homoptera: Aphididae) on cotton.
J. Pest Sci.
86
:
167
172
.
Gergs,
A.,
Zenker
A.,
Grimm
V.
and
Preuss
T.G.
2013
.
Chemical and natural stressors combined: From cryptic effects to population extinction.
Sci. Rep.
3
:
2036
.
Gonzalez-Megias,
A.
and
Gomez
J.M.
2003
.
Consequences of removing a keystone herbivore for the abundance and diversity of arthropods associated with a cruciferious shrub.
Ecol. Entomol.
28
:
299
308
.
Henry,
Y.,
Renault
D.
and
Colinet
H.
2018
.
Hormesis-like effect of mild larval crowding on thermotolerance in Drosophila flies.
J. Exp. Biol.
221
:
jeb169342
.
Hu,
L.-L.,
Liu
Y.,
Xu
H.-F.
and
Zhi
L.-S.
2004
.
Intra- and interspecific relationship of Myzus persicae (Sulzer) and Lipaphis erysimi (Kaltenbach) on cabbage.
Entomol. J. East China
13
:
77
80
.
Hullé,
M.,
Chaubet
B.,
Turpeau
E.
and
Simon
J.
2020
.
Encyclop'Aphid: A website on aphids and their natural enemies.
Entomol. Gen.
40
:
97
101
.
Iwabuchi,
T.
and
Urabe
J.
2012
.
Competitive outcomes between herbivorous consumers can be predicted from their stoichiometric demands.
Ecosphere
3
:
7
.
Jordan,
H.R.
and
Tomberlin
J.K.
2017
.
Abiotic and biotic factors regulating inter-kingdom engagement between insects and microbe activity on vertebrate remains.
Insects
8
:
1
19
.
Kaplan,
I.
and
Denno
R.F.
2007
.
Interspecific interactions in phytophagous insects revisited: A quantitative assessment of competition theory.
Ecol. Lett.
10
:
977
994
.
Karban,
R.
1986
.
Interspecific competition between folivorous insects on Erigeron glaucus.
Ecology
67
:
1063
1072
.
Klepsatel,
P.,
Prochazka
E.
and
Gáliková
M.
2018
.
Crowding of Drosophila larvae affects lifespan and other life-history traits via reduced availability of dietary yeast.
Exp. Gerontol.
110
:
298
308
.
Li,
H.-B.,
Wu
K.-M.,
Xu
Y.,
Yang
X.-R.,
Yao
J.,
Sun
S.-L.,
Li
X.-Y.
and
Jiang
H.-Y
2008
.
Dynamic analysis of population of cotton aphids in the south of Xinjiang.
Xinjiang Agric. Sci.
45
:
670
675
.
Li,
Y.
and
Akimoto
S.
2021
.
Self and non-self-recognition affects clonal reproduction and competition in the pea aphid.
Proc. Roy. Soc. B-Biol. Sci.
288
:
20210787
.
Lü,
J.,
Cao
T.-T.,
Wang
L.-P.,
Jiang
M.-X.
and
Cheng
J.-A.
2011
.
Comparative study on density related intra- and inter-specific effects in Laodelphax striatellus (Fallen) and Nilaparvata lugens (Stål).
Acta Ecol. Sinica
31
:
4680
4688
.
Lü,
Z.-Z.,
Tian
C.-Y.
and
Song
Y.-D.
2002
.
Relationship between Aphis gossypii and Acyrthosiphon gossypii on cotton in Xinjiang.
China Cotton
29
:
11
12
.
Magneville,
C.,
Ratz
T.,
Richardson
J.
and
Smiseth
P.T.
2018
.
No evidence of sibling cooperation in the absence of parental care in Nicrophorus vespilloides.
Evolution
72
:
2803
2809
.
Marchioro,
C.A.
and
Foerster
L.A.
2011
.
Development and survival of the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Yponomeutidae) as a function of temperature: Effects on the number of generations in tropical and subtropical regions.
Neotrop. Entomol.
40
:
533
541
.
Marchioro,
C.A.
and
Foerster
L.A.
2016
.
Biotic factors are more important than abiotic factors in regulating the abundance of Plutella xylostella L., in southern Brazil.
Rev. Bras. Entomol.
60
:
328
333
.
Meng,
L.
and
Li
B.-P.
2000
.
Effect of intra-specific competition on population dynamic of the cotton aphid, Aphis gossypii.
J. Xinjiang Agric. Univ.
23
:
42
44
.
Mohammed,
A.A.A. H.,
Desneux
N.,
Monticelli
L.S.,
Fan
Y.-J.,
Shi
X.-Y.,
Guedes
R.N.C.
and
Gao
X.-W.
2019
.
Potential for insecticide-mediated shift in ecological dominance between two competing aphid species.
Chemosphere
226
:
651
658
.
Moran,
N.A.
and
Whitham
T.G.
1990
.
Interspecific competition between root-feeding and leaf-feeding aphids mediated by host-plant resistance.
Ecology
71
:
1050
1058
.
Morimoto,
J.,
Nguyen
B.,
Dinh
H.,
Than
A.T.,
Taylor
P.W.
and
Ponton
F.
2019
.
Crowded developmental environment promotes adult sex-specific nutrient consumption in a polyphagous fly.
Front. Zool.
16
:
1
11
.
Morimoto,
J.,
Pizzari
T.
and
Wigby
S.
2016
.
Developmental environment effects on sexual selection in male and female Drosophila melanogaster.
PLoS ONE
11
:
e0154468
.
Mueller,
L.D.,
Guo
P.-Z.
and
Ayala
F.J.
1991
.
Density-dependent natural selection and trade-offs in life history traits.
Science
253
:
433
435
.
Naselli,
M.,
Biondi
A.,
Garzia
T.G.,
Desneux
N.,
Russo
A.,
Siscaro
G.
and
Zappala
L.
2017
.
Insights into food webs associated with the South American tomato pinworm.
Pest Manag. Sci.
73
:
1352
1357
.
Pan,
H.-P.,
Ge
D.-Q.,
Wang
S.-L.,
Wu
Q.-J.,
Xu
B.-Y.,
Xie
W.
and
Zhang
Y.-J.
2010
.
Replacement of B biotype Bemisia tabaci by Q biotype B. tabaci in some areas of Beijing and Hebei.
Plant Prot.
36
:
40
44
.
Qu,
Y.-Y.,
Ullah
F.,
Luo
C.,
Monticelli
L. S.,
Lavoir
A.-V.,
Gao
X.-W.,
Song
D.-L.
and
Desneux
N.
2020
.
Sublethal effects of beta-cypermethrin modulate interspecific interactions between specialist and generalist aphid species on soybean.
Ecotox. Environ. Safe
206
:
111302
.
Reis,
S.F.S.,
Von Zuben
C.J.
and
Godoy
W.A.C.
1999
.
Larval aggregation and competition for food in experimental populations of Chrysomya putoria (Wied.) and Cochliomyia macellaria (F.) (Dipt., Calliphoridae).
J. Appl. Entomol.
123
:
485
489
.
Reitzl,
S.R.
and
Trumble
J.T.
2002
.
Interspecific and intraspecific differences in two Liriomyza leafminer species in California.
Entomol. Exp. Appl.
102
:
101
113
.
Savopoulou-Soultani,
M.,
Papadopoulos
N.T.,
Milonas
P.
and
Moyal
P.
2012
.
Abiotic factors and insect abundance.
Psyche J. Entomol.
2012
:
1
2
.
Soares,
S.d.A.
2013
.
The role of competition in structuring ant communities: A review.
Oecologia Australis
17
:
271
281
.
Than,
A.T.,
Ponton
F.
and
Morimoto
J.
2020
.
Integrative developmental ecology: A review of density-dependent effects on life-history traits and host–microbe interactions in nonsocial holometabolous insects.
Evol. Ecol.
34
:
1
22
.
Thirakhupt,
V.
and
Araya
J.E.
1992
.
Interaction between bird cherry-oat aphid (Rhopalosiphum padi) and English grain aphid (Macrosiphum avenae) (Homoptera: Aphididae) on ‘Abe’ wheat.
J. Plant Dis. Prot.
99
:
201
208
.
Tsurim,
I.,
Silberbush
A.,
Ovadia
O.,
Blaustein
L.
and
Margalith
Y.
2018
.
Inter- and intraspecific density-dependent effects on life history and development strategies of larval mosquitoes.
PLoS ONE
8
:
e57875
.
Utsumi,
S.,
Ando
Y.
and
Miki
T.
2010
.
Linkages among trait-mediated indirect effects: A new framework for the indirect interaction web.
Popul. Ecol.
52
:
485
497
.
van Veen,
F.F.J.,
Morris
R.J.
and
Godfray
H.C.J.
2006
.
Apparent competition, quantitative food webs, and the structure of phytophagous insect communities.
Annu. Rev. Entomol.
51
:
187
208
.
Villemereuil,
P.B.
and
Lopez-Sepulcre
A.
2011
.
Consumer functional responses under intra- and inter-specific interference competition.
Ecol. Model
222
:
419
426
.
Wang,
J.-L.,
Li
H.-G.,
Feng
Z.-G.
and
Zheng
C.-Y.
2011
.
Interspecific competition between Frankliniella occidentalis and Thrips tabaci on purple cabbage.
Scientia Agric. Sinica
44
:
5006
5012
.
Wu,
N.,
Zhang
Y.-D.,
Cai
X.-H.,
Shi
Y.-H.,
Han
R.
and
Wang
J.-G.
2020
.
Studies on the activities of related enzymes of Aphis gossypii after feeding cotton damaged by Acyrthosiphon gossypii.
Xinjiang Agric. Sci.
57
:
2056
2064
.
Xu,
R.-M.
1987
.
Entomological population ecology.
Beijing Normal Univ. Press
,
China
.
Yan,
W.-J.,
Wang
J.-G.,
Zhang
Y.-D.
and
Wu
N.
2019
.
Selection behavior of Acyrthosiphon gossypii and Aphis gossypii to cotton plants under the stress of aphids feeding.
Xinjiang Agric. Sci.
56
:
52
60
.
Yan,
W.-J.,
Zhang
Y.-D.,
Wu
N.
and
Wang
J.-G.
2020
.
Selective response of Acyrthosiphon gossypii and Aphis gossypii to their honeydew.
Jiangsu Agric. Sci.
48
:
130
134
.
Yan,
W.-T.,
Qiu
G.-S.,
Zhou
Y.-S.,
Zhang
H.-J.,
Zhang
P.,
Liu
C.-L.
and
Zheng
Y.-C.
2010
.
Interspecific domino effects of three major pernicious mites in apple orchard.
J. Fruit Sci.
27
:
815
818
.
Yao,
Y.-S.
2017
.
Interspecific pattern change of Aphis gossypii and Acyrthosiphon gossypii and its influencing factors in Southern Xinjiang cotton-growing region.
PhD Dissertation. China Agricultural Univ.
,
Beijing
.
Yi,
H.,
Wang
K.-G.,
Zhang
L.-Y.,
Lei
Z.-R.,
Luo
H.-W.,
Lian
Z.-M.
and
Zhou
G.-Q.
2014
.
Density-dependent effect of Liriomyza trifolii at immature stage and interspecific competition with Liriomyza sativae.
Scientia Agric. Sinica
47
:
4269
4279
.
Zhang,
Y.-D.,
Wu
N.,
Cai
X.-H.,
Shi
Y.-H.
and
Wang
J.-G.
2020
.
Effects of Acyrthosiphon gossypii on physiology, biochemistry and related defense enzymes of cotton.
Xinjiang Agric. Sci.
57
:
2065
2074
.
Zhao,
W.-C.,
Lou
Y.-G.,
Cheng
J.-A.
and
Zhu
Z.-R.
2001
.
Intra-and interspecific relationship of Nilaparvata lugens (Stål) and Sogatella furcifera (Horváth) on various rice varieties.
Acta Ecol. Sinica
21
:
629
638
.
Zhao,
X.,
Reitz
S.R.,
Yuan
H.,
Lei
Z.,
Paini
D.R.
and
Gao
Y.
2017
.
Pesticide-mediated interspecific competition between local and invasive thrips pests.
Sci. Rep.
7
:
40512
.
Zheng
C.-Y.,
Feng
Z.-G.,
Wang
Y.-H.
and
Wang
S.-F.
2012
.
Study on the interspecific competition between Bemisia tabaci and Trialeurodes vaporariorum under the same habitat.
J. Agric.
2
:
20
24
.

Author notes

2Co-first authors.