Biological response of Rhopalosiphum padi and Sipha flava (Hemiptera: Aphididae) changes over generations

1 Introduction

Livestock farming is socioeconomically important for Brazil. The sector employs more than 1.5 million people and generated approximately R$357.4 billion in 2022 (CNA 2023). An important characteristic of Brazilian livestock farming, which guarantees low production costs, is that most herds are raised in pastures (Dias-Filho 2016) without supplemental feed. However, it is estimated that 80 % of the cultivated pasture areas in Central Brazil are in some state of degradation (Carvalho et al. 2017).

Pasture degradation refers to a process of sharp and continuous drop in productivity (Dias-Filho 2017), caused by the biotic and/or abiotic disturbances that interrupt normal growth of a forage crop (Batunacun et al. 2021), such as attack by insect pests (Dias-Filho 2011; Fonseca et al. 2016). Insect pests are considered the main biotic problem of pastures, considerably reducing the quantity and quality of forage, interfering with plant persistence, and consequently accelerating degradation processes (Congio et al. 2020; Valério and Nakano 1987).

The main groups of insect pests in pastures in Brazil are spittlebugs (Hemiptera: Cercopidae), stink bugs (Hemiptera: Miridae) and aphids (Hemiptera: Aphididae) (Auad et al. 2012; Fonseca et al. 2014, 2016]; Paiva et al. 2020; Silva et al. 2019). Aphids damage plants by sucking sap, injecting toxic substances and acting as virus vectors (Sturza et al. 2012). Rhopalosiphum padi (Linnaeus) and Sipha flava (Forbes) are species widely distributed in tropical and subtropical regions, associated with different species of the Poaceae (Auad et al. 2009; Hentz and Nuessly 2004; Lumbierres et al. 2004; Oliveira et al. 2009a; Parchen and Auad 2016; Sturza et al. 2012; Wilson 2019).

Some studies of the biological aspects of R. padi and S. flava were conducted in Brazil, investigating, for example, the life expectancy and fertility parameters of S. flava in Pennisetum purpureum Schumach. (Poaceae) (Oliveira et al. 2009b; Parchen and Auad 2016), and of R. padi in Urochloa ruziziensis (R.Germ. & C.M.Evrard) Crins (Poaceae) (Auad et al. 2009). These studies brought significant results and contributions to the study area of aphids in pastures, helping to guide management strategies. However, the assessment and interpretation of the effects of pest outbreaks on the persistence of forages in pastures is still limited due to the limited knowledge of biology, life cycles and mobility of pests in different forages (Zydenbos et al. 2011), which includes the effect of successive generations of insects on their bioecological and behavioral aspects, as most research on insect responses has referred to a single generation (Moura et al. 2022; Seo et al. 2020).

Multiple generational effects in insect life table parameters sometimes are used to evaluate the nutritional components of host plants in artificial diets, resistance of transgenic plants, effects of elevated CO₂ and temperature, and effects on biological control agents in mass rearing (Chen et al. 2011; Gao et al. 2014; Guo et al. 2013; Li et al. 2022; Smith et al. 2007). For R. padi and S. flava multigenerational effects on biological parameters, including the life table, are not known. These studies could help in understanding, at least in part, the reasons for the conflicting results of the biological performance of aphids determined under laboratory conditions.

The objective of the present work was to evaluate the biological aspects and life table of R. padi in brachiaria (U. ruziziensis) and S. flava in elephant grass (P. purpureum) during five consecutive generations in the laboratory.

2 Materials and methods

3 Results

4 Discussion

There are different variables that influence the development, longevity and fertility of aphids, including temperature and type of food (Hong et al. 2019; Park et al. 2017; Seo et al. 2020). However, most studies do not take into account that the influence of these variables may be different throughout the generations of the insect. Biological studies applied over generations of target organisms allow a better understanding of the adaptation of aphid species, for example, to their host plants and to abiotic conditions.

In the present research it was shown that S. flava and R. padi demonstrated significant differences in performance depending on the generation, even under ideal host plant and climatic conditions, as determined in previous studies (Auad et al. 2009; Oliveira et al. 2009a). These results contrast with those found in previous studies with other insect species, for example, in biological studies of Mahanarva fimbriolata (Stål) (Hemiptera: Cercopidae) for three generations in the laboratory, the results were similar for all generations (Garcia et al. 2006), which, in our case, gives a reliable support to validate the adaptation of the insect to the technique used to rear the species in the laboratory. Similarly, the life table parameters of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) remained relatively stable over five successive generations, between temperatures of 27–31 °C, indicating the insect’s adaptation to these temperatures across generations (Guo et al. 2013).

Our results suggest that S. flava undergoes changes in biological variables across generations. In our study, the first generation exhibited a longer nymphal period and increased longevity, resulting in a longer biological cycle compared to subsequent generations. In contrast, previous studies on this species reported a shorter life cycle (from birth to death) and higher fertility in the first generation (Oliveira et al. 2009b; Parchen and Auad 2016) when compared with the current research.

From the second generation onwards, the nymphal development of S. flava accelerated. The shorter feeding time of nymphs, and consequently less nutrient accumulation, may have led to shorter adult longevity. However, the shortening of the nymphal period and longevity over generations appears to be a positive adaptation for the species as there are no significant effects on nymphal survival. Furthermore, in the fifth generation, high production of nymphs and high values in the life table parameters (rm, R ₀ and λ) were observed with shorter time between the generations and population doubling time. The duration of biological development in phytophagous insects is an important factor to help evaluate host quality, which over the course of development may or may not indicate low nutritional quality (Oliveira 2012; Parchen and Auad 2016). Furthermore, the action of abiotic factors can act in conjunction with nutrition, influencing the duration of development periods of the insects. Here we observed that over five generations in the laboratory, the biotic potential of S. flava increased.

R. padi, in general, presented unfavorable biological characteristics (longevity, nymphal survival, and fecundity) for the second, fourth and fifth generations, as well as a lower biotic potential for these generations. It suggests that the development of R. padi on brachiaria may be negatively affected over generations. In other studies, with this species, with the same host plant and under the same climatic conditions (Auad et al. 2009; Oliveira et al. 2009a; Parchen and Auad 2016) a shorter duration of the nymphal phase, a faster population doubling time, and higher nymphal survival were reported for the first generation compared to our findings.

Comparing some biological characteristics of the two aphid species, it was observed, for example, that the number of nymphs produced per female were approximately 15 % higher for the fifth generation of S. flava, in relation to the first, and about 90 % lower for the fifth generation of R. padi. Variations in life table parameters also were recorded with clear and specific variations among generations between the two species studied. The innate capacity to increase in number followed the following order for S. flava rm (generation = G): G1 = G2 = G3 < G4 + G5 and for R. padi rm: G1 > G2 < G3 > G4 > G5, suggesting a greater adaptation for S. flava and an unfavorable relationship for R. padi, respectively, across the generations. These differences observed in the biology of S. flava and R. padi can be explained, in part, by the characteristics of each aphid species. Aphids are organisms sensitive to changes in temperature, humidity, quality of the host plant and each species can present different responses in relation to the biotic and abiotic factors and the intrinsic characteristics of the insect.

Our results are different from the results obtained for the first generation of these same species in other studies conducted under similar conditions (climatic conditions and host plant) (Auad et al. 2009; Oliveira et al. 2009a; Parchen and Auad 2016). We attribute these differences to the intrinsic genetic characteristics of the first generation collected in the original infestation, as in the other studies, the first generation was obtained from aphid colonies raised under controlled conditions. This suggests the need for standardization of the individuals to be used in aphid biological studies.

A joint analysis of the data presented here allows us to hypothesize that the characteristics of populations collected in the original infestation (first generation) influence the results of the biological studies carried out in the laboratory with S. flava and R. padi, as significant differences were observed in the biological parameters and life table parameters of aphids over multiple generations. Thus, the standardization of the generation to be used and the origin of the insects to be used in the studies (from the field or from laboratory colonies) are important factors in obtaining more reliable and comparable biological information between the studies carried out by the different research groups of insects with the same aphid species. Finally, multigeneration studies are important tools for understanding the responses of S. flava and R. padi, especially in relation to the adaptation of these species to host plants over multiple generations. Such studies can be informative in genetic improvement programs of forages, for example those programs aimed at enhancing genetic resistance to aphid species.