Journal of Threatened Taxa | www.threatenedtaxa.org | 26 August 2024 | 16(8): 25758–25764

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

https://doi.org/10.11609/jott.9171.16.8.25758-25764

#9171 | Received 30 May 2024 | Final received 30 July 2024 | Finally accepted 03 August 2024

A short-term impact of enriched CO₂ [eCO₂] on select growth performance of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) and its host plant Gossypium barbadense L. (Malvaceae)

A.A. Abu ElEla Shahenda ¹ & Wael M. ElSayed ²

^1,2 Department of Entomology, Faculty of Science, Cairo University, Egypt 12613.

¹ Graduate School of Agricultural Science, Tohoku University, Sendai, Miyagi 980‑8572, Japan.

¹ shosho_ali76@yahoo.com (corresponding author),² wael_elsayed88@yahoo.com

Editor: A.J. Solomon Raju, Andhra University, Visakhapatnam, India. Date of publication: 26 August 2024 (online & print)

Citation: A.A.A.E. Shahenda & W.M. ElSayed (2024). A short-term impact of enriched CO₂ [eCO₂] on select growth performance of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) and its host plant Gossypium barbadense L. (Malvaceae). Journal of Threatened Taxa 16(8): 25758–25764. https://doi.org/10.11609/jott.9171.16.8.25758-25764

Copyright: © Shahenda & ElSayed 2024. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

Funding: Self-funded.

Competing interests: The authors declare no competing interests.

Author details: Dr. Wael M. ElSayed is an associate professor of Ecology and the director of the Ecology, Biodiversity and Pollution Laboratory, College of Science, Cairo University since 2017. The broad research interest is ecology, aquatic pollution, community ecology, population dynamics and conservation of different organismal groups. Formerly, he was a visiting professor at Hokkaido University, Japan and worked on investigating the stress of changing environment on biodiversity across different localities in Japan and Egypt. Also, His research interests lie in the ecology of Acrididae and Carabidae. Dr. Shahenda Abu ElEla is an adjunct associate professor of Ecology and expertise in environmental pollution, global climate change, forestry ecology, atmospheric pollution, and anthropogenic disturbances. Her research is focusing on studying the impact of enriched CO₂ and enriched Ozone (O₃) on plant-insect interactions and monitoring the changes in insect biodiversity under different climatic conditions. Also, her research interests lie in the ecology of some Orthopteran species in Kanazawa and Sendai, Japan especially the lesser known Tetrigidae.

Author contributions: All the authors contributed in the field study; AA Shahenda conceived and designed the study; AA conducted the measurements and collected the data; AA Shahenda and ElSayed M. Wael wrote the manuscript draft; ElSayed Wael conducted statistical analysis, reviewed and edited the manuscript drafts; all authors approved the final draft and contributed significantly.

Acknowledgements: The authors are highly grateful to Prof. Dr. Michio Kondoh (Department of Ecological Developmental Adaptability Life Sciences, Tohoku University) and Prof. Dr. Masatoshi Hori (Graduate School of Agricultural Science, Tohoku University) for their hospitality and kindness in providing facilities to write and complete the draft of the manuscript. The authors are thankful to Dr. Hiromi Uno (associate professor, Watershed Ecology Lab, Aobayama Campus, Graduate School of Life Sciences, Tohoku University, Japan) for her time and efforts in revising the Japanese abstract.

Abstract: Natural interactions between herbivorous insect pests and their host plants are expected to be altered significantly as atmospheric CO₂ concentrations (aCO₂) continue to rise according to climate change scenario. The possible effect of enriched CO₂ (eCO₂) environments on these interactions is under attention. To better understand such effects on select insect growth parameters; early (3^rd) and penultimate (6^th) instar larvae of the Cotton Leaf Worm Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae), reared on the cotton plant leaves Gossypium barbadense L. (Malvacae) grown under either ambient (aCO₂ = 350 ppm) or enriched (eCO₂ = 700 ppm) atmospheres were investigated.

Keywords: Ambient CO₂, CO₂-enriched atmosphere, growth parameters.

Introduction

The ever-increasing combustion of fossil fuels, such as energy generation in coal-fired power plants, cement plants, oil refineries, and land-use changes has contributed towards the increase of atmospheric CO₂ concentration (aCO₂) (Houghton et al. 1992; Leakey et al. 2009; Goufo et al. 2014). The aCO₂ level has gone from the pre-industrial value of 280 ppm to a current level of 418 ppm (December 2022) where a high aCO₂ concentration is a big risk to human health, for example, it can trigger respiratory illnesses when the aCO₂ concentration is over 600 ppm (NOAA 2022; Åhlén et al. 2023).

The rate of change of aCO₂ levels has accelerated with models predicting that by the middle of this century; the aCO₂ levels will escalate to 550 ml L^–1 and expected to rise to about 800 ml L^–1 by the end of this century (Long & Ort 2010; Feng & Cheng 2014).

Increasing amount of CO₂ in the atmosphere affects the global climate temperature, which can have an adverse effect on all life forms on this planet (Bazzaz 1990; Abu ElELa & ElSayed 2018; Ashok et al. 2022). Thus, numerous studies have focused on understanding the CO₂ effects on various aspects of plant growth, productivity, and survival in crops. Only a few studies have dealt with the nutritional quality of food crops and even fewer studies on the health-promoting phytochemicals in food crops (Rajashekar 2018).

Little is known about the effects of the eCO₂ environments, which are anticipated to exist in the next century, on natural plant-insect herbivore interactions. Because of the crucial role of CO₂ in photosynthesis, the expected increase in global aCO₂ levels will exert a significant influence on the biological systems.

Climate change has a marked impact on the biology and population ecology of insect pests with direct impact on the physiology and behavior of the insect (Berrigan 2000). Insect life cycle is influenced by climate, this includes total duration of life span, fecundity, mortality, and genetic adaptation (Helmuth et al. 2002; Hoffmann et al. 2003; Stillman 2003; Abu ElEla & ElSayed 2018). Moreover, the indirect effects could be observed through the impact on host plant, parasitoids, and predators of insect pests (Manimanjari & Rao 2022). In addition to this, eCO₂ will affect the quality of foliage and in turn influence the potential herbivorous behavior of the insect pest.

Often, plant species grown in eCO₂ environments have a higher foliar water content than those grown under aCO₂ conditions (Wong 1979; Fajer et al. 1991; Lincoln et al. 1993), potentially enhancing insect herbivore performance (Scriber 1977, 1979). However, plant species reared in eCO₂ environments also showed comparatively reduced nitrogen concentrations in leaves (Wong 1979; Williams et al. 1981; Fajer et al. 1991; Lincoln et al. 1993).

Studies dealing with lepidopteran larvae have revealed that insect herbivores consistently respond to changes in plant foliar quality induced by eCO₂ environments by consuming more foliage (Osbrink et al. 1987; Johnson & Lincoln 1990; Fajer et al. 1991, Abu ElEla & ElSayed 2018). It is assumed that insects consume more foliage to compensate for reduced foliar nitrogen concentrations (Slansky & Feeny 1977). Some species showed a lower rate of larval development or even incomplete development of larvae; decreased fecundity , and increased mortality (Osbrink et al. 1987; Fajer 1989; Fajer et al. 1991).

In Egypt, one of the most important fiber crops is the cotton, Gossypium barbadense L. (Malvaceae), and because of its economic importance; the phytophagous insect Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) larva is considered as one of the major and injurious noctuid predator of cotton in Egypt (Abu ElEla & ElSayed 2018).

Laboratory feeding studies and growth chamber experiments have provided useful information about the responses of insect herbivores to specific foliage or plant species grown under aCO₂ and eCO₂ conditions (Caulfield & Bunce 1994; Abu ElEla & El Sayed 2018; Rao et al. 2012; Manimanjari & Rao 2022).

Indeed, there is a shortage of knowledge and the information pertaining to the possible influence of eCO₂ regime on natural interactions between the noctuid pest, S. littoralis (Boisd.), and its host plants especially those of economic importance (such as G. barbadense L.) are fragmentary. Thus, the aim of this research work is to focus some light on some select biological and life cycle parameters of S. littoralis (Boisd.) fed with cotton plant leaves, G. barbadense L. var. Super Giza 85, grown under both aCO₂ (350 ppm) & eCO₂ (700 ppm).

Materials and Methods

The study was conducted at the Laboratory of Applied Entomology, Cairo University, Egypt. Cotton seeds of Gossypium barbadense L. (var. Super Giza 85) were obtained from Seeds Bank at the Ministry of Agriculture, Cairo, Egypt. Five seeds/4-liter soil were germinated in plastic pots containing sand & clay through summer season from May to September and were irrigated regularly by tap water. These pots were placed inside designated cuboid open top chambers (80 l x 80 w x 80 h cm). Natural lighting, ranging from 600 μ mol-2s^-1 to 2,000 μ mol-2s^-1, was primarily used. Although white fluorescent Philips^® lamps, automatically programmed were used to maintain a 12D: 12L light regime, added additional light at 1,000 μmol-2s^-1 were used when light levels fell below 600 μmol-2s^-1 (Carlson & Bazzaz 1980). These chambers containing the G. barbadense L. var. Super Giza saplings were exposed to aCO₂ (350 ppm) and eCO₂ (700ppm) regimes. Plants were grown for 30 days before offering the foliage as a diet for the experimental insect.

Leaf nutritional quality

Leaf nutritional quality was measured at 30 days and 45 days by chemical analyses of contents for total nitrogen, total carbohydrates, and phenolic compounds. Chemical analysis was done for total amino acids according to the method described by Russell (1944), total carbohydrates according to Streeter & Jeffers (1979), and total phenolic compounds according to the method by Jindal & Singh (1975).

Growth conditions of S. littoralis (Boisd.)

Eggs were obtained from the females of S. littoralis (Boisd.) reared from standard laboratory colony maintained at the Department of Entomology, Cairo University since 2000s. Two groups of 50 eggs were placed in plastic petridishes (Ø 14 cm) with moist paper towel strips taped to the lid to maintain suitable air humidity. One group of hatched larvae was offered cotton plant leaves grown in aCO₂ regime while the other group was fed on leaves grown in eCO₂ regime.

Hatched larvae were kept in growth chambers with a 14 h day: 10 h night light regime and 25°C day: 20°C night temperature regime. Fresh leaves were provided every other day. Each CO₂ treatment had 20 replicates of 10 larvae per petridish. Larvae were reared & fed from the 1^st instar till last instar and ceased feeding as they reached prepupal stage.

The 3^rd (hereafter considered as the early instar) and the 6^th (considered as the penultimate instar) (Image 1) were used as main larval instars in this experiment due to their potential herbivory (ElEla & ElSayed 2018). Usually, S. littoralis (Boisd.) shows six larval instars, however, we treated the 3^rd larval instar as an early instar since the 1^st and 2^nd instars showed less herbivory attitude to cotton leaves (personal observations) and only nibbling of soft leaves could be observed. Also, the 6^th instar showed strong voracious tendency to consume leaves until reaching the prepupal stage which showed unambiguous cessation of feeding.

The number and average fresh weights of newly formed prepupae were recorded. The prepupae were then placed in sieved, sterilized, and moistened wood dust to proceed in forming the pupal cases. Percentage pupation and mean pupal duration were recorded. By the emergence of adults, number of emerged adults, longevity, and sex ratio were recorded. The freshly emerged adults were fed on 10% sugary solution (sucrose solution) and were offered small fresh twigs bearing leaves of Nerium oleander L. to serve as ovipositional sites for adult females.

Statistical analysis

The effects of CO₂ regimes on the select larval parameters were evaluated by one-way Analysis of Variance (ANOVA). The differences between the mean values of treatments were determined by Duncan’s multiple range test. Treatment means were compared and separated using least significant difference (LSD) at p <0.05. All statistical analyses were computed by using SPSS version 16.0.

Results and Discussion

Data depicted in Table 1 revealed insignificant difference (p >0.05) between mean larval duration for the 3^rd and 6^th larval instars fed cotton plant leaves grown under aCO₂ and eCO₂ regimes. In general, the larval duration for either 3^rd (early) and 6^th (penultimate) larval instars were slightly greater for those fed cotton leaves grown in eCO₂ regime. However, significant difference (p <0.05) in the percentage larval survival was observed between the two regimes (Table 1). The percentage larval survival was greater for larvae fed aCO₂ grown cotton leaves compared to those fed enriched-grown leaves (Table 1). It was clear that relatively greater number of larvae fed aCO₂ could successfully complete the larval duration when compared to those fed eCO₂-grown cotton leaves. Also, it seemed that larval mortality could be related to the nutritional deficiency that resulted from reduced foliar nitrogen levels in eCO₂ grown plants (Brooks & Whittaker 1999; Abu ElEla & ElSayed 2018).

Although we found that penultimate S. littoralis (Boisd.) larvae consumed additional eCO₂-grown cotton leaves (based on personal observations), they showed relatively slower growth rate with longer larval duration (Table 1). Moreover, these penultimate larvae produce pupae with relatively lighter fresh weights compared to those produced from the penultimate instars fed aCO₂-grown leaves (Table 1). This could be attributed to their inability to fully compensate for the diet which is relatively poor in nitrogen as they were forced to metabolize food at higher flow rates, such as when they consumed additional eCO₂-grown leaves, they could not effectively process enough food for the compensation of relatively lower nitrogen concentrations (Rogers et al. 1994; Davis & Potter 1989; Abu ElEla & ElSayed 2018). However, it is far from precise to generalize this finding among other insect pest species since Hughes & Bazzaz (1997) reported no effect on populations of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) fed with Ascelpias syriaca L. (Asclepiadaceae) grown in eCO₂ atmosphere.

Prolonged larval duration, such as those induced by the eCO₂-grown diets in this study, may prevent larvae from completing development in climatically limited environments with short growing seasons (Davis & Potter 1989; Watt et al. 1995). Reduced growth rates and increased larval duration of the larvae fed eCO₂-grown leaves may also increase their exposure to predators & parasitoids (Carlson & Bazzaz 1980; Davis & Potter 1989; Ottman et al. 2001).

As penultimate larvae reached the prepupal stage, the interruption of feeding was noticeable (Montezano et al. 2019). The prepupae started to build the pupal case which made it possible to observe metamorphosis and determine the end of the prepupal period which was relatively short duration (1–2 days) in both the CO₂ regime.

The recorded prepupal fresh weight showed significant difference (p <0.05) between the aCO₂ and eCO₂ regimes (Table 1). Pre-pupae resulted from penultimate larvae fed cotton leaves grown in aCO₂ regime were remarkably heavier than those resulted from larvae fed eCO₂-grown leaves (Table 1).

Although the mean percentage pupation was found to be lower for larvae fed cotton leaves grown in eCO₂ regime (84.66 ± 4.83) rather than from aCO₂ regime (90.53 ± 1.486), insignificant difference (p > 0.05) was observed between the two regimes (Table 1). However, the mean pupal duration showed significant difference (p <0.05) for pupae resulting from larvae fed on cotton leaves grown in aCO₂ regime (Table 1) where pupae of ambient condition showed relatively prolonged duration compared to pupae of enriched condition.

Moreover, significant difference (p <0.05) was observed in the mean pupal fresh weight between the two CO₂ regimes where pupae resulted from larvae fed grown cotton leaves grown at aCO₂ regime showed greater fresh weight (2.583 ± 0.036) compared to those fed eCO₂-grown leaves (Table 1). Robinson et al. (2012) stated that growth rates when consuming high CO₂ foliage are reduced, and duration increased, resulting in lower prepupal, pupal, and adult weights. 

Adults emerged from larvae reared on ambient grown cotton leaves showed a significant (p <0.05) greater mean percentage emergence compared to those fed eCO₂-grown cotton leaves (Table 1). The mortality rate for adults resulted from larvae fed eCO₂-grown leaves was much greater (ca. 15%) compared to adults emerged from larvae fed aCO₂-grown leaves (Table 1).

More males emerged, but the Co₂ regimes did not influence the sex ratio as insignificant difference (p >0.05) was observed between the CO₂regimes for both sexes (Table 1).

Measures of plant quality during the present study are thus of importance in understanding natural interactions between herbivorous insect and its host plant species under eCO₂ environment since insect feeding and growth is a function of both the variation since diverse plant species respond differently to atmospheric eCO₂ alterations in foliage quality composition (Rao et al. 2012; Abu ElEla & ElSayed 2018; Manimanjari & Rao 2022). Increase in aCO₂ levels can cause increases in plant growth rates, and changes in the physical and chemical composition of the plant tissues (Stockle 1992; Sudderth 2005; Abu ElEla & ElSayed 2018).

Treatment of cotton plants with eCO₂ regime caused a significant alteration in plant quality in term of chemical characteristics (Table 2). It was observed that nitrogen content was drastically reduced in cotton leaves grown in eCO₂ concentration to show 50% less nitrogen contents (0.281 ± 0.029 mg g^-1d.wt) compared to nitrogen contents in leaves grown at aCO₂ regime (Table 2). In accordance with this finding, other studies have also showed that many plant species grown under eCO₂ condition showed a reduction in leaf nitrogen content (Stitt & Krapp 1999; Rao et al. 2012; Manimanjari & Rao 2022).

Significant difference (p <0.05) in total foliar carbohydrates was observed between the two CO₂ regimes (Table 2). In the present study, eCO₂ typically increases the concentration of foliar total carbohydrates (42.82 ± 0.381 mg g^-1d.wt) which showed 15% greater concentration than total carbohydrates concentration in foliar grown in aCO₂ (Table 2).

Results shown in Table 2 showed that the total concentration of phenolic contents were higher under eCO₂. A significant difference (p <0.05) in the total phenolic contents was observed between the two CO₂ treatments (Table 2) where the total phenolic contents in cotton leaves increased by more than double its value under eCO₂ compared to the contents of phenolics in aCO₂-grown cotton leaves. This improvement in plant secondary metabolites could be attributed to increased total non-structural carbohydrates (TNC) as suggested by Ibrahim & Jafaar (2012). Phenolics are considered as one of the most important groups of secondary metabolites and bioactive compounds in plant species (Kim et al. 2005) and increased levels of CO₂ concentrations can influence the levels of total phenolics (Fine et al. 2006).

The eCO₂ exhibited a significant impact on cotton plant by altering the biochemical constituents of the foliage such as reduced nitrogen content, increased phenolics, increased carbon, C:N, and total carbohydrates. It was clear that eCO₂ amplified decreases in foliar total nitrogen, causing substantial increases in foliar C:N ratio (Zvereva & Kozlov, 2006) which in turn affect the growth & development of the phytophagous early & penultimate instars, and subsequent stages of S. littoralis (Boisd.).

Consuming more eCO₂-grown leaves is an unambiguous indicator that eCO₂ reduces insect growth rates by altering the chemical and physical properties of foliage. In our study, cotton leaves grown in eCO₂ regime possessed relatively high total carbohydrates and low nitrogen content (Table 2). Consequently, increasing C:N which causes apparent increase in the consumption of relatively low-quality food to meet critical nutrient limitations which is referred to as “compensatory feeding” and may portend greater herbivore damage to both managed & natural ecosystems as CO₂ continues to increase (Cornelissen 2011).

Conclusion

It was clear that the phytophagous pests respond in an immediate fashion to the leaves grown in eCO₂. Larvae fed aCO₂-grown cotton leaves showed shorter duration, comparatively heaviest prepupae & pupae, and greatest percentage of adult emergence. On the other hand, larvae fed eCO₂- grown cotton leaves showed relatively longer duration and lighter prepupae & pupae with smaller percentage adult emergence. Consequently, the population dynamics of S. littoralis (Boisd.) and the nutritional quality of the host plant, G. barbadense L., could be influenced by the future increase of aCO₂ levels.

Table 1. Select parameters of larval stages of Spodoptera littoralis (Boisd.) fed the leaves of Gossypium barbadense L. grown in ambient (aCO2 = 350 ppm) and enriched (eCO2 = 700 ppm) CO2 regimes.

* Results followed by different letters are significantly different (p <0.05)

Insect parameters	CO2 treatment
	aCO2 (350 ppm)	eCO2 (700 ppm)
Larval stage Larval duration (day) 3^rd instar (early) 6^th instar (penultimate) Percentage total larval survival (%)	3.6 ± 0.116^a* 4.5 ± 0.27^a 90.83 ± 0.19^a	3.83 ± 0.27^a 4.83 ± 0.253^a 83 ±2.27^b
Prepupal stage Prepupal fresh weight (g.)	2.27 ± 0.158^a	1.27 ± 0.014^b
Pupal stage Percentage pupation (%) Pupal fresh weight (g) Pupal duration (day)	90.53 ± 1.486^a 2.583 ± 0.036^a 11.33 ± 0.026^a	84.66 ± 4.83^a 1.87 ± 0.027^b 7.66 ± 0.068^b
Adult stage Percentage adult emergence (%) Sex ratio Male (%) Female (%)	96.27 ± 2.21^a 56.33 ± 3.82^a 46.67 ± 4.38^a	82.24 ± 3.98^b 58.33 ± 3.21^a 44.33 ± 3.82^a

Table 2. Select nutritional quality of cotton plant leaves of Gossypium barbadense L. grown in ambient (aCO2 = 350 ppm) and enriched (eCO2 = 700 ppm) CO2 regimes.

Leaf nutritional quality(mg g^-1d.wt)	CO2 Treatment
	aCO2 (350 ppm)	eCO2 (700 ppm)
Total carbohydrates	36.49 ± 0.19^a*	42.82 ± 0.381^b
Total nitrogen	0.565 ± 0.046^a	0.281 ± 0.029^b
Phenolic compounds	0.645 ± 0.012^a	1.524 ± 0.016^b

* Results followed by different letters are significantly different (p <0.05).

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