Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Influence of Temperature on Intra- and Interspecific Resource Utilization within a Community of Lepidopteran Maize Stemborers

  • Eric Siaw Ntiri ,

    ensiaw@gmail.com

    Affiliations International Centre of Insect Physiology and Ecology, Nairobi, Kenya, Unit of Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

  • Paul-Andre Calatayud,

    Affiliations International Centre of Insect Physiology and Ecology, Nairobi, Kenya, UMR IRD 247 Laboratoire Evolution, Génomes, Comportement et Ecologie, Diversité, Ecologie et Evolution des Insectes Tropicaux, CNRS, Gif-sur-Yvette, France and Université de Paris-Sud, Orsay, France

  • Johnnie Van Den Berg,

    Affiliation Unit of Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

  • Fritz Schulthess,

    Affiliation Postfach 508, Chur, Switzerland

  • Bruno Pierre Le Ru

    Affiliations International Centre of Insect Physiology and Ecology, Nairobi, Kenya, UMR IRD 247 Laboratoire Evolution, Génomes, Comportement et Ecologie, Diversité, Ecologie et Evolution des Insectes Tropicaux, CNRS, Gif-sur-Yvette, France and Université de Paris-Sud, Orsay, France

Influence of Temperature on Intra- and Interspecific Resource Utilization within a Community of Lepidopteran Maize Stemborers

  • Eric Siaw Ntiri, 
  • Paul-Andre Calatayud, 
  • Johnnie Van Den Berg, 
  • Fritz Schulthess, 
  • Bruno Pierre Le Ru
PLOS
x

Abstract

Competition or facilitation characterises intra- and interspecific interactions within communities of species that utilize the same resources. Temperature is an important factor influencing those interactions and eventual outcomes. The noctuid stemborers, Busseola fusca and Sesamia calamistis and the crambid Chilo partellus attack maize in sub-Saharan Africa. They often occur as a community of interacting species in the same field and plant at all elevations. The influence of temperature on the intra- and interspecific interactions among larvae of these species, was studied using potted maize plants exposed to varying temperatures in a greenhouse and artificial stems kept at different constant temperatures (15°C, 20°C, 25°C and 30°C) in an incubator. The experiments involved single- and multi-species infestation treatments. Survival and relative growth rates of each species were assessed. Both intra- and interspecific competitions were observed among all three species. Interspecific competition was stronger between the noctuids and the crambid than between the two noctuids. Temperature affected both survival and relative growth rates of the three species. Particularly at high temperatures, C. partellus was superior in interspecific interactions shown by higher larval survival and relative growth rates. In contrast, low temperatures favoured survival of B. fusca and S. calamistis but affected the relative growth rates of all three species. Survival and relative growth rates of B. fusca and S. calamistis in interspecific interactions did not differ significantly across temperatures. Temperature increase caused by future climate change is likely to confer an advantage on C. partellus over the noctuids in the utilization of resources (crops).

Introduction

Maize (Zea mays L.) is one of the most important cereal crops worldwide, utilized as human food, animal feed and industrial raw materials [1, 2]. In developed countries such as in the US (the largest producer of maize), a greater part of total production is used for animal feed, with an increased proportion utilized for biofuel [1, 2]. However, in developing countries such as in Africa, 95% of total maize production, mostly by small scale farms, is used for human food. In addition, maize production in this region is fraught with a myriad of challenges including pests, diseases, drought and nutrient deficiency [1].

Lepidopteran stemborers such as the indigenous noctuids Busseola fusca (Fuller) and Sesamia calamistis (Hampson) and the exotic crambid Chilo partellus (Swinhoe) attack the maize crop in East and southern Africa [3, 4]. Depending on the elevation they may occur as single species or communities of mixed species attacking maize stems in the same field [58]. For instance, in Kenya, the composition of these stemborer communities varies with elevation. Busseola fusca is the predominant species in the highlands characterised by low temperatures, while C. partellus is the most abundant species in the hot lowlands. In contrast, S. calamistis is present in low numbers at all elevations. It is only at the mid-elevations do the three species occur as a mixed community, but the predominance of a species may vary with location and season [7, 9, 10].

The common use of a limited resource by several species for their survival predisposes them to interact competitively [1113] or facilitatively [11, 14, 15]. Some of the most important questions in ecology concern intra- and interspecies interactions in mixed communities [16]. For instance, the role of competition in the organisation of insect communities despite being questioned by several authors [11, 1719], has been resuscitated by two crucial reviews on the subject which presented strong evidence for the dominance of competition in phytophagous insect communities [11, 20].

Temperature is the most crucial abiotic factor for insects, as it directly drives their life processes [2126]. It also influences resource utilisation, intra- and inter-specific interactions and limits their geographic distribution [24, 2732]. For example, competitive interactions between the burying beetles Nicrophorus orbicollis Say and N. defodiens Mannerheim (Coleoptera: Silphidae), when feeding on the same carcass, was reported to be temperature dependent [33]. In an experiment involving the seed beetle Stator limbatus (Horn) (Coleoptera: Chrysomelidae), cooler temperatures conferred a competitive advantage on smaller males, which out-competed larger ones in reaching a potential mate [34]. Future temperature increase due to climate change [35] is predicted to affect the type and intensity of species interactions [28, 3638]. For example, changes in temperature was reported to influence the intensity of intraspecific competition by the grasshopper Camnula pellucida (Scudder) (Orthoptera: Acrididae) [39]. Surprisingly few studies have been carried out to assess the effect of possible future temperature increases on the competitive and facilitative interactions within communities of insects utilising the same resource [38, 40].

Reports of competitive displacement of B. fusca and Chilo orichalcociliellus Strand by C. partellus from overlap in resource use have been reported in South Africa [41, 42] and in the coastal region of Kenya [43], respectively, but the mechanisms behind the species displacements are not known. The temperature requirements of each of these stemborers have been well studied [25, 26], but the effects of temperature on their interactions are yet to be elucidated.

This paper reports on the kind of intra- and interspecific interactions that characterise resource utilization (maize infestation) by communities of B. fusca, S. calamistis and C. partellus and the effect of temperature on these interactions, as well as discusses the potential impact of climate changes on these interactions.

Materials and Methods

Plants and insects

Seeds of the H513 hybrid maize variety (Simlaw, Kenya Seed Company, Nairobi, Kenya) were planted in plastic pots (12 cm in height x 13 cm in diameter), in a greenhouse at the campus of the International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya (S 01°13'17.8", E 036°53'45.0"). Mean temperatures were approximately 31/17°C (day/night) with a 12:12 h (L:D) photoperiod. Maize plants at the sixth leaf stage, (the earliest maize plant stage found to be infested in the field) were used in the experiments.

Second instar larvae of B. fusca (Bf), C. partellus (Cp) and S. calamistis (Sc) were obtained from colonies reared at the Animal Rearing and Containment Unit (ARCU) at icipe, Nairobi, Kenya. Larvae were reared in plastic jars (16.5 cm length x 9cm diameter) filled with 200 ml of artificial diet of Onyango and Ochieng’-Odero [44]. The diet contained vitamins, maize leaf powder, Brewer’s yeast, bean powder and anti-microbial agents such as ascorbic acid. Agar was also added to enable liquid diet to solidify and also to hold moisture. The jars were covered with tissue paper and tightly closed with perforated lids with galvanized mesh, to prevent larvae escape and kept in a holding room with a temperature of 26±1°C and RH of 60±5%. Colonies were rejuvenated twice a year with field collected larvae.

Surrogate stems

In a preliminary trial, larvae-infested plants kept in an incubator (Sanyo MIR 554, Japan) deteriorated after only 5–7 days. Thus, a method using surrogate stems filled with artificial diet was used (Fig 1). These surrogate stems consisted of a 30cm piece of PVC pipe with a diameter of 5cm. Each piece was cut into equal halves to allow opening of the stem for observation of the larvae. The halves were held together with masking tape. One end of the pipe was covered with parafilm® and reinforced with masking tape. The pipe was wrapped in aluminium foil and fastened with a rubber band leaving one end uncovered. This was done to prevent leakage of hot liquid diet when dispensed later into pipes. The pipes were then filled with the aforementioned artificial diet of Onyango and Ochieng’-Odero [44]. Once the diet had solidified in the tubes after 24 hours, the masking tapes and three quarters of the aluminium foil covering the tubes were removed from top to bottom, leaving only one quarter of the pipe covered.

thumbnail
Fig 1. PVC surrogate stem for rearing stemborer larvae on artificial diet.

(a) halves of pipe before they are joined, (b) full pipe after halves have been joined.

http://dx.doi.org/10.1371/journal.pone.0148735.g001

The following three experiments were conducted:

Experiment 1. The influence of maize and surrogate stems on the development of stemborer larvae

This experiment involved a single-species infestation treatment, conducted on potted plants and surrogate stems. Both substrates were each infested with 12 second instar larvae of the same species of each species (Cp, Bf, and Sc), using a small camel hair brush (size 2). A density of 12 larvae per surrogate stem is representative of that found on maize in the field at the beginning of the infestation (B. Le Ru, unpublished). The infested plants were covered with a netted metal frame tied with rubber bands at the base of the pots to prevent larvae from escaping. For the surrogate stems, the free ends were plugged with cotton wool after infestation with larvae. Each treatment was replicated twenty times on both maize plants and surrogate stems. The surrogate stems were placed in jars to keep them upright. The experiment was undertaken under varying temperatures in a semi-natural condition in a greenhouse during the hot season, from December to March (min. temp., 13°C, max. temp., 27°C, and mean of 20°C). This period corresponded to the growing season of maize in most parts of Kenya. The temperature was recorded with a HOBO® Temp/RH data logger (Onset, USA). After 30 days, all maize stems were dissected and surrogates stems opened to record the number and the mass of surviving larvae of each species.

Experiment 2. Influence of larval density on intra-specific interactions

This experiment was conducted to investigate intraspecific interactions at low and high density infestations. For the low density infestation, surrogate stems were infested with six second instar larvae (6L) and for the high density infestation, stems were infested with twelve second instar larvae (12L) of the same species of each species (Cp, Bf, and Sc). The surrogate stems were then plugged with cotton wool after infestation. The surrogate stems were placed in jars to keep them upright and were then kept in an incubator (Sanyo MIR 554, Japan) at a constant temperature of 25°C, the optimum temperature for all three species [25, 26], air humidity of 70±10% and LD of 12:12. Each treatment was replicated twenty times. The number and mass of surviving larvae of each species were recorded from surrogate stems after 30 days.

Experiment 3. Influence of different constant temperatures on intra- and interspecific interactions

This experiment involved single- and multi-species infestation treatments conducted with surrogate stems. The single-species infestation treatments involved infestation of surrogate stems with 12 larvae of the same species of each species (Cp, Bf and Sc). The multi-species infestation treatment involved infestation of surrogate stems with six larvae of each species for the Cp+Bf, Cp+Sc, Bf+Sc pairings, and four larvae of each species for the three-species treatment, Cp+Bf+Sc. The surrogate stems were then plugged with cotton wool after infestation. The stems were placed in jars to keep them upright. This experiment was conducted in incubators (Sanyo MIR 554, Japan) at four constant temperatures of 15, 20, 25, and 30°C, air humidity of 70±10% and LD of 12:12. Each treatment was replicated twenty times. After 30 days, surrogates stems were opened to record the number and the mass of surviving larvae of each species.

Data analysis

Survival rates (i.e., the number of larvae alive after 30 days) and relative growth rates (RGR) were used as the response variables. The RGR for each species was calculated following the equation of Ojeda-Avila et al.[45]:

RGR for communities was calculated as the sum of the RGR of all species in that community. Survival rates for each treatment were analysed using the generalized linear model with binomial error structure. Odd Ratios with a 95% confidence interval (O.R. [95%CI]) were calculated for the comparison made between treatments from the GLM results obtained. The differences between RGR of species from each treatment, was analysed via analysis of variance (ANOVA). The level of significance was set at 5%. Means were separated with the Student-Newman-Keuls (SNK) test. The RGR data were first tested for normality of their distribution by a Kolmogorov-Smirnov test and for homoscedasticity by the Bartlett’s test. All analyses were carried out in R [46].

Results

Experiment 1. Influence of maize and surrogate stems on the development of stem borer larvae

For each species, survival rates were significantly higher on surrogate stems than maize plants (Fig 2A). The survival of each species was about double in surrogate stems compared to maize plants. RGRs were also significantly higher on surrogate stems than on maize plants for C. partellus and S calamistis. It increased by a factor of 1.5 to 2 for each species respectively on surrogate stems compared to maize plants (Fig 2B). However, the RGR of B. fusca did not differ significantly between surrogate stems and maize plants.

thumbnail
Fig 2.

Survival (a) and relative growth rates (b) of Chilo partellus (Cp), Busseola fusca (Bf) and Sesamia calamistis (Sc) larvae on maize and surrogate stems under varying temperatures. Means (± SE) with different letters are significantly different at 5% level according to the GLM for survival and the Student-Newman-Keuls test for relative growth rates.

http://dx.doi.org/10.1371/journal.pone.0148735.g002

Experiment 2. Influence of larval density on intra-specific interactions between stem borer larvae

The survival rates were significantly lower for high infestation than low infestation levels for B. fusca [O.R. = 1.8 (1.06–3.21), p = 0.03], C. partellus [O.R. = 1.9 (1.1–3.47), p = 0.02] and S. calamistis [O.R. = 2.0 (1.1–3.9), p = 0.03] (Fig 3A). For both infestation levels, C. partellus had the highest survival rate, while S. calamistis had the lowest survival rates. However, there were variations in the RGRs of the three species at the different densities. The RGRs were significantly higher for high infestation than low infestation for C. partellus (F = 4.9, p = 0.03) and S. calamistis (F = 6.9, p = 0.01), whereas for B. fusca it was significantly higher (F = 19.3, p<0.001) for low infestation than high infestation levels (Fig 3B). Also, while B. fusca had the highest RGR at low infestation level, S. calamistis had the highest RGR at high infestation level (Fig 3B).

thumbnail
Fig 3.

Survival (a) and relative growth rates (b) of Chilo partellus (Cp), Busseola fusca (Bf) and Sesamia calamistis (Sc) at low density (6L) and high density (12L) infestation at 25°C. Means (± SE) with different letters are significantly different at 5% level according to the GLM for survival and the Student-Newman-Keuls test for relative growth rates.

http://dx.doi.org/10.1371/journal.pone.0148735.g003

Experiment 3. Influence of different constant temperatures on intra- and interspecific interactions

a) The effect of temperature on survival and RGR of B. fusca, C. partellus and S. calamistis as single-species.

For each species, larval survival in the single-species treatments varied significantly between temperatures (Fig 4A). For B. fusca, it was highest at 20°C and lowest at 25°C. For C. partellus, it was highest at 20°C and similar among the other temperatures, while for S. calamistis it was higher at 15°C and 20°C than 25°C and 30°C (Table 1). RGR of each species was lowest at 15°C (Fig 5A). For S. calamistis, it was similar at 20°C and 30°C and highest at 25°C, while for B. fusca, it was highest at 30°C. For C. partellus, the highest RGR was recorded at 20°C, whereafter it decreased with increasing temperature (Fig 5A, Table 2).

thumbnail
Fig 4.

Comparison of survival of Chilo partellus (Cp), Busseola fusca (Bf) and Sesamia calamistis (Sc) larvae as single-species (a) and between borer species in multi-species communities at different constant temperatures (b-e). Means (± SE) with different letters are significantly different at 5% level. GLM (binomial).

http://dx.doi.org/10.1371/journal.pone.0148735.g004

thumbnail
Fig 5.

Comparison of the relative growth rates (RGR) of Chilo partellus (Cp), Busseola fusca (Bf) and Sesamia calamistis (Sc) larvae as single-species (a) and between borer species in multi-species communities at different constant temperatures (b-e). Means (± SE) with different letters are significantly different at 5% level according to the Student-Newman-Keuls test.

http://dx.doi.org/10.1371/journal.pone.0148735.g005

thumbnail
Table 1. Results of GLM analysis comparing larval survival of each single-species at different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t001

thumbnail
Table 2. Results of ANOVA comparing relative growth rates of each single-species at different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t002

b) Comparison of survival and RGR of B. fusca, C. partellus and S. calamistis in multi-species communities under different constant temperatures.

Survival was higher for C. partellus than its companion species at all temperatures (Fig 4B and 4C, e and Table 3). In pairings with B. fusca and S. calamistis, survival was similar between the two species at all temperatures except at 15°C (Fig 4D). In pairings with C. partellus, the crambid had significantly higher RGRs than B. fusca at all temperatures except at 30°C (Fig 5B) and also higher than S. calamistis at 15°C and 20°C (Fig 5C). In pairings involving both noctuids, RGRs did not vary significantly between the two species regardless of the temperature (Fig 5D), except for the 3-species pairing at 25°C where S. calamistis had a higher RGR than B. fusca (Fig 5E, Table 4).

thumbnail
Table 3. Results of GLM analysis comparing larval survival between borer species in multi-species communities at different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t003

thumbnail
Table 4. Results of ANOVA comparing relative growth rates between borer species in multi-species communities at different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t004

c) Comparison of survival and relative growth rates between single and multi-species communities of B. fusca, C. partellus and S. calamistis at different constant temperatures.

When significant, survival and RGR of single species communities were higher than total survival and RGR of the corresponding multi-species communities. Between 20–30°C, survival of B. fusca, and C. partellus singly tended to be higher than total survival of the corresponding multi-species communities. For S. calamistis, it was higher than that of multi-species communities at 15° and 20°C, and to a lesser extent at 25° and 30°C (Fig 6A, Table 5). Likewise between 20° and 30°C, RGRs of single-species communities of C. partellus, B. fusca, and to a lesser extent of S. calamistis tended to be higher than total RGRs of the corresponding multi-species communities (Fig 6B, Table 6).

thumbnail
Fig 6.

Comparative survival (a) and RGR (b) between single-species and multi-species communities of Chilo partellus (Cp), Busseola fusca (Bf) and Sesamia calamistis (Sc) under different constant temperatures. Statistical comparisons were only made between single- and the corresponding multi-species pairings (see Tables 5 and 6).

http://dx.doi.org/10.1371/journal.pone.0148735.g006

thumbnail
Table 5. Results of GLM analysis comparing survival between single-species and multi-species communities under different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t005

thumbnail
Table 6. Results of ANOVA comparing the relative growth rates between single-species and multi-species communities under different constant temperatures.

http://dx.doi.org/10.1371/journal.pone.0148735.t006

Discussion

For each species, survival was reduced when the larval density doubled. Also, when reared together with one or several species, survival and RGR of each species tended to decrease compared to the single-species treatment. Thus, the intra- and interspecific interactions between the stemborer species tested in this study indicated competitive resource utilization. An inverse effect of density on species fitness and their interactions is an established ecological fact [4749] and a typical characteristic of spatially restricted insects such as Lepidoptera living inside a stem and exploiting the same resources [11, 19, 20, 50]. Cereal stemborers in East Africa constitute an extreme case of interactions for resource utilisation. Their larvae have developed a close association with their host plants [51] as they coexist with a “restricted” resource, available over a short period of time (2 to 3 months), with the most nutritious stage between 2 to 8 weeks and with unreliable availability of suitable hosts because drought spells commonly occur in the region. All these characteritics make cereal stemborers a good model for testing the competition theory [11, 20, 52].

Interspecific competition was more pronounced than intraspecific competition, especially when C. partellus was involved, with the outcomes skewed asymmetrically towards the crambid. This indicates a higher fitness of the crambid compared to the two noctuids. This confirms the asymmetry of interspecific competition outcomes in phytophagous insects [11, 20, 53]. Thus in favourable regions where the crambid co-occurs with either one or both noctuids in infesting maize or any cereal crop, the crambid will likely dominate over the other two species.

The superior competitive abilities of C. partellus over other species have been reported from other field and laboratory studies. In South Africa, C. partellus was reported to be superior to B. fusca in colonizing ratoon sorghum and its population build-up occurred faster [41]. Furthermore, a comparison of life traits using five grasses showed that the invasive C. partellus laid more viable eggs, its larvae consumed more food and had a higher survival and shorter developmental rate than the native C. orichalcociliellus [54]. Various studies have described the superior competitive abilities of invasive over native species. For instance, the superior competitive abilities of several invasive species as a key factor for their successful establishment has been well documented [55]. The proficiency in both interference and exploitative competition was also reported to confer a superior ability on the invasive Argentine ant, Linepithema humile Mayr (Hymenoptera: Formicidae) over native species [56].

The competition-relatedness hypothesis states that closely related species will compete stronger than distantly related species [11, 57]. In contrast, in the present study, competition was stronger between distant-related species (noctuids and crambid) than between the two noctuids belonging to the same sub-tribe. Similarly, results from a meta-analysis concluded that distant-relatedness rather than phylogenetic similarity determined the strength of competition in insects [20]. The present study thus confirms others that disputes the competition-relatedness hypothesis [5860].

This study demonstrated that temperature is an important factor influencing the interactions between the noctuids and the crambid. Thereby, the competitive abilities of each of the species depended on its temperature tolerance limits for development. While high temperatures favoured C. partellus, the two noctuids had highest survival rates under lower temperatures. Likewise, as shown previously [25, 26], the development rate of the three species increased with temperature but this was more pronounced for C. partellus and S. calamistis than B. fusca. In the field, while C. partellus and B. fusca dominate within a limited thermal tolerance at the high and low temperature extremes, respectively, S. calamistis has a wider thermal tolerance by co-occuring with the two species along these temperature gradients [7, 9, 10].

The role of temperature in influencing varied competitive abilities of interacting species has been reported from three Drosophila species [61], between small and large seed beetle species Stator limbatus [34], the invasive fruit fly Bactrocera invadens Drew, Tsuruta & White over the indigenous fruit fly, Ceratitis cosyra (Walker) (Diptera: Tephritidae) [62] and two invasive leaf miner flies Liriomyza sativae Blanchard and L. trifolii (Burgess) (Diptera: Agromyzidae) [63]. In these studies, the competitive abilities of one of the competing species was enhanced by either low or high temperatures. Similar trends of temperature influence have been reported from competition studies involving plants [64], fish [6567] and bacterivorous ciliates [68].

Several studies have been conducted to assess the potential impacts of climate change on various life history parameters of insects such as their population dynamics, survival and mass and their distribution [28, 6973]. However, few studies exist on the effects of temperature increase on the interactions of species using the same resources [39]. Results of the present study suggest that a future increase in temperature would confer a greater competitive ability on C. partellus than the two noctuid species. Similarly, temperature-dependent models predicted that C. partellus will expand into the highlands where B. fusca presently dominates [26]. With its better competitive abilities, C. partellus is likely to outcompete the two noctuids in the highlands and become the dominant species. In fact, C. partellus has already been recorded from highlands in Kenya and cooler regions of South Africa, and in some cases it has become the dominant species [4, 7, 9, 10, 41, 42]. This is also likely to increase the level of damage to cereal crops in these high elevation regions, given that C. partellus causes more injury than B. fusca on maize in some regions [5, 7]. Similar observations of a potential increase in crop damages by other insect pests, caused by temperature increase due to climate change, have been reported [28, 74, 75].

As shown by higher survival and RGRs for C. partellus and S. calamistis, surrogate stems were a good alternative to maize plants. Although the RGRs were not significantly higher in surrogates stems compared to maize plants for B. fusca, the use of surrogate stems for this species was also a good alternative to maize plants since its survival increased almost by twofold in surrogtae stems compared to maize plants. In general, insects tend to perform better on artificial than on natural diets since artificial diets possess optimum levels of nutrients and vitamins [76]. However in nature, early instars of C. partellus and B. fusca migrate by “ballooning off” the plant [77, 78], which is not possible when surrogate stems are used. Thus, whether the higher survival on surrogate stems were due to lower mortality or reduced migration could not be determined with the present experimental set-up. Still, surrogate stems are more stable than maize stems or potted plants because they do not deteriorate that easily and are thus ideal for such studies. Similarly, higher survival of S. calamistis reared on artificial diet than on maize stem cuttings was reported by other authors [79].

This study highlights the knowledge gap in our understanding of temperature effects on biodiversity, especially interactions between species utilizing the same resources. Besides temperature, rainfall is another abiotic factor which could influence interactions within stemborer communities [8084]. In addition, biotic factors such as density dependence [48], level of multi-species infestations in the field and oviposition-site selection of the female adults [8587] could also influence stemborer species interactions. Further studies which elucidate the influences of these factors will enable a better understanding of the impact of stemborer interactions on cereal crop damage, especially under future climate scenarios and contribute to the development of possible mitigation and adaption strategies.

Acknowledgments

We acknowledge the technical assistance provided by staff of the IRD-NSBB project in icipe, especially Boaz Musyoka. We also thank the stemborer rearing unit of the ARCU-icipe for the rearing and supply of insect larvae for this experiment and the bio-statistics unit of icipe for statistical support.

Author Contributions

Conceived and designed the experiments: BLR ESN PAC. Performed the experiments: ESN BLR. Analyzed the data: ESN. Contributed reagents/materials/analysis tools: BLR ESN PAC. Wrote the paper: ESN BLR PAC JVDB FS.

References

  1. 1. International Institute of Tropical Agriculture. Maize 2009. Available: http://www.iita.org/maize. Accessed 10 April 2015.
  2. 2. Ranum P, Peña-Rosas J, Garcia-Casal M. Global maize production, utilization, and consumption. Ann N Y Acad Sci. 2014;1312:105–12. doi: 10.1111/nyas.12396. pmid:24650320
  3. 3. Seshu Reddy K. Maize and sorghum: East Africa. In: Polaszek A, editor. African cereal stem borers: economic importance, taxonomy, natural enemies and control. Wallingford: CAB International; 1998. p. 25–8.
  4. 4. Kfir R, Overholt W, Khan Z, Polaszek A. Biology and management of economically important lepidopteran cereal stem borers in Africa. Annu Rev Entomol. 2002;47(1):701–31.
  5. 5. Van Den Berg J, Van Rensburg J, Pringle K. Comparative injuriousness of Busseola fusca (Lepidoptera: Noctuidae) and Chilo partellus (Lepidoptera: Pyralidae) on grain sorghum. Bulletin of Entomological Research. 1991;81(02):137–42.
  6. 6. Tefera T. Lepidopterous stem borers of sorghum and their natural enemies in eastern Ethiopia. Tropical Science. 2004;44(3):128–30.
  7. 7. Ong’amo GO, Le Ru BP, Dupas S, Moyal P, Calatayud P-A, Silvain J-F. Distribution, pest status and agro-climatic preferences of lepidopteran stem borers of maize in Kenya. Annales de la Société Entomologique de France. 2006;42(2):171–7.
  8. 8. Krüger W, Van Den Berg J, Van Hamburg H. The relative abundance of maize stem borers and their parasitoids at the Tshiombo irrigation scheme in Venda, South Africa. South African Journal of Plant and Soil. 2008;25(3):144–51.
  9. 9. Guofa Z, Overholt WA, Mochiah MB. Changes in the distribution of lepidopteran maize stemborers in Kenya from the 1950s to 1990s. International Journal of Tropical Insect Science. 2001;21(04):395–402.
  10. 10. Ong’amo GO, Le Ru BP, Dupas S, Moyal P, Muchugu E, Calatayud P-A, et al. The role of wild host plants in the abundance of lepidopteran stem borers along altitudinal gradient in Kenya. Annales de la Société Entomologique de France. 2006;42(3–4):363–70.
  11. 11. Denno RF, McClure MS, Ott JR. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu Rev Entomol. 1995;40(1):297–331.
  12. 12. Agrawal AA. Future directions in the study of induced plant responses to herbivory. Entomologia Experimentalis et Applicata. 2005;115(1):97–105.
  13. 13. Leibold MA. The niche concept revisited: mechanistic models and community context. Ecology. 1995;76(5):1371–82.
  14. 14. Stachowicz JJ. Mutualism, Facilitation, and the Structure of Ecological Communities Positive interactions play a critical, but underappreciated, role in ecological communities by reducing physical or biotic stresses in existing habitats and by creating new habitats on which many species depend. Bioscience. 2001;51(3):235–46.
  15. 15. Bruno JF, Stachowicz JJ, Bertness MD. Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution. 2003;18(3):119–25.
  16. 16. Sutherland WJ, Freckleton RP, Godfray HCJ, Beissinger SR, Benton T, Cameron DD, et al. Identification of 100 fundamental ecological questions. Journal of Ecology. 2013;101(1):58–67.
  17. 17. Connell JH. On the prevalence and relative importance of interspecific competition: evidence from field experiments. American Naturalist. 1983;122:661–96.
  18. 18. Karban R. Interspecific competition between folivorous insects on Erigeron glaucus. Ecology. 1986;67:1063–72.
  19. 19. Gurevitch J, Morrow LL, Wallace A, Walsh JS. A meta-analysis of competition in field experiments. American Naturalist. 1992;140:539–72.
  20. 20. Kaplan I, Denno RF. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecology Letters. 2007;10(10):977–94. pmid:17855811
  21. 21. Logan J, Wollkind D, Hoyt S, Tanigoshi L. An analytic model for description of temperature dependent rate phenomena in arthropods. Environmental Entomology. 1976;5(6):1133–40.
  22. 22. Lactin DJ, Holliday N, Johnson D, Craigen R. Improved rate model of temperature-dependent development by arthropods. Environmental Entomology. 1995;24(1):68–75.
  23. 23. Bezemer TM, Jones TH, Knight KJ. Long-term effects of elevated CO2 and temperature on populations of the peach potato aphid Myzus persicae and its parasitoid Aphidius matricariae. Oecologia. 1998;116(1–2):128–35.
  24. 24. Dangles O, Carpio C, Barragan A, Zeddam J-L, Silvain J-F. Temperature as a key driver of ecological sorting among invasive pest species in the tropical Andes. Ecological Applications. 2008;18(7):1795–809. pmid:18839773
  25. 25. Khadioli N, Tonnang Z, Ong'amo G, Achia T, Kipchirchir I, Kroschel J, et al. Effect of temperature on the life history parameters of noctuid lepidopteran stem borers, Busseola fusca and Sesamia calamistis. Annals of Applied Biology. 2014;165(3):373–86.
  26. 26. Khadioli N, Tonnang Z, Muchugu E, Ong'amo G, Achia T, Kipchirchir I, et al. Effect of temperature on the phenology of Chilo partellus (Swinhoe)(Lepidoptera, Crambidae); simulation and visualization of the potential future distribution of C. partellus in Africa under warmer temperatures through the development of life-table parameters. Bulletin of Entomological Research. 2014;104(06):809–22.
  27. 27. Howe R. Temperature effects on embryonic development in insects. Annu Rev Entomol. 1967;12(1):15–42.
  28. 28. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Bezemer TM, Brown VK, et al. Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology. 2002;8(1):1–16.
  29. 29. Sporleder M, Kroschel J, Quispe MRG, Lagnaoui A. A temperature-based simulation model for the potato tuberworm, Phthorimaea operculella Zeller (Lepidoptera; Gelechiidae). Environmental Entomology. 2004;33(3):477–86.
  30. 30. Hodkinson ID. Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev. 2005;80(3):489–513. pmid:16094810
  31. 31. Speight MR, Hunter MD, Watt AD. Ecology of insects: concepts and applications. Second ed: John Wiley & Sons Ltd; 2008. 628 p.
  32. 32. Damos P, Savopoulou-Soultani M. Temperature-driven models for insect development and vital thermal requirements. Psyche. 2012;2012:13pp. doi: 10.1155/2012/123405.
  33. 33. Wilson D, Knollenberg W, Fudge J. Species packing and temperature dependent competition among burying beetles (Silphidae, Nicrophorus). Ecological Entomology. 1984;9(2):205–16.
  34. 34. Moya-Laraño J, El-Sayyid MET, Fox CW. Smaller beetles are better scramble competitors at cooler temperatures. Biology Letters. 2007;3(5):475–8. pmid:17638675
  35. 35. Intergovernmental Panel on Climate Change. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team, Pachauri R.K. and Meyer L.A. (eds.)]. Geneva, Switzerland: IPCC, 2014.
  36. 36. Cammell M, Knight J. Effects of climatic change on the population dynamics of crop pests. Advances in Ecological Research. 1992;22:117–62.
  37. 37. Buse A, Dury S, Woodburn R, Perrins C, Good J. Effects of elevated temperature on multi‐species interactions: the case of Pedunculate Oak, Winter Moth and Tits. Functional Ecology. 1999;13(s1):74–82.
  38. 38. Tylianakis JM, Didham RK, Bascompte J, Wardle DA. Global change and species interactions in terrestrial ecosystems. Ecology Letters. 2008;11(12):1351–63. pmid:19062363
  39. 39. Laws AN, Belovsky GE. How will species respond to climate change? Examining the effects of temperature and population density on an herbivorous insect. Environmental Entomology. 2010;39(2):312–9. doi: 10.1603/EN09294. pmid:20388258
  40. 40. Gilman SE, Urban MC, Tewksbury J, Gilchrist GW, Holt RD. A framework for community interactions under climate change. Trends in Ecology & Evolution. 2010;25(6):325–31.
  41. 41. Kfir R. Competitive displacement of Busseola fusca (Lepidoptera: Noctuidae) by Chilo partellus (Lepidoptera: Pyralidae). Annals of the Entomological Society of America. 1997;90(5):619–24.
  42. 42. Rebe M, Van Den Berg J, McGeoch M. Colonization of cultivated and indigenous graminaceous host plants by Busseola fusca (Fuller)(Lepidoptera: Noctuidae) and Chilo partellus (Swinhoe)(Lepidoptera: Crambidae) under field conditions. African Entomology. 2004;12(2):187–99.
  43. 43. Ofomata V, Overholt W, Huis Av, Egwuatu R, Ngi‐Song A. Niche overlap and interspecific association between Chilo partellus and Chilo orichalcociliellus on the Kenya coast. Entomologia Experimentalis et Applicata. 1999;93(2):141–8.
  44. 44. Onyango F, Ochieng’-Odero J. Continuous rearing of the maize stem borer Busseola fusca on an artificial diet. Entomologia Experimentalis et Applicata. 1994;73(2):139–44.
  45. 45. Ojeda-Avila T, Woods HA, Raguso R. Effects of dietary variation on growth, composition, and maturation of Manduca sexta (Sphingidae: Lepidoptera). Journal of Insect Physiology. 2003;49(4):293–306. pmid:12769983
  46. 46. R Development Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2014. http://www.r-project.org/
  47. 47. Applebaum S, Heifetz Y. Density-dependent physiological phase in insects. Annu Rev Entomol. 1999;44(1):317–41.
  48. 48. Agnew P, Hide M, Sidobre C, Michalakis Y. A minimalist approach to the effects of density‐dependent competition on insect life‐history traits. Ecological Entomology. 2002;27(4):396–402.
  49. 49. Pascual S, Callejas C. Intra-and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bulletin of Entomological Research. 2004;94(04):369–75.
  50. 50. Stiling PD, Strong DR. Weak competition among spartina stem borers, by means of murder. Ecology. 1983;64:770–8.
  51. 51. Zilli A, Ronkay L, Fibiger M. Noctuidae Europaeae. Vol. 8. Apameini. Entomological Press Sorø; 2005.
  52. 52. Stokes K, Stiling P. Indirect competitive effects of stemborers on a gall community. Entomologia Experimentalis et Applicata. 2015;154(1):23–7.
  53. 53. Inbar M, Eshel A, Wool D. Interspecific competition among phloem-feeding insects mediated by induced host-plant sinks. Ecology. 1995;76:1506–15.
  54. 54. Ofomata V, Overholt W, Lux S, Van Huis A, Egwuatu R. Comparative studies on the fecundity, egg survival, larval feeding, and development of Chilo partellus and Chilo orichalcociliellus (Lepidoptera: Crambidae) on five grasses. Annals of the Entomological Society of America. 2000;93(3):492–9.
  55. 55. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, et al. The population biology of invasive species. Annual Review of Ecology and Systematics. 2001;32:305–32.
  56. 56. Holway DA. Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology. 1999;80(1):238–51.
  57. 57. Violle C, Nemergut DR, Pu Z, Jiang L. Phylogenetic limiting similarity and competitive exclusion. Ecology Letters. 2011;14(8):782–7. doi: 10.1111/j.1461-0248.2011.01644.x. pmid:21672121
  58. 58. Best R, Caulk N, Stachowicz J. Trait vs. phylogenetic diversity as predictors of competition and community composition in herbivorous marine amphipods. Ecology Letters. 2013;16(1):72–80. doi: 10.1111/ele.12016. pmid:23066869
  59. 59. Venail PA, Narwani A, Fritschie K, Alexandrou MA, Oakley TH, Cardinale BJ. The influence of phylogenetic relatedness on species interactions among freshwater green algae in a mesocosm experiment. Journal of Ecology. 2014;102(5):1288–99.
  60. 60. Alexandrou MA, Cardinale BJ, Hall JD, Delwiche CF, Fritschie K, Narwani A, et al. Evolutionary relatedness does not predict competition and co-occurrence in natural or experimental communities of green algae. Proceedings of the Royal Society B: Biological Sciences. 2015;282(1799):20141745. doi: 10.1098/rspb.2014.1745. pmid:25473009
  61. 61. Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS. Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. Journal of Animal Ecology. 1998;67(4):600–12.
  62. 62. Rwomushana I, Ekesi S, Ogol CK, Gordon I. Mechanisms contributing to the competitive success of the invasive fruit fly Bactrocera invadens over the indigenous mango fruit fly, Ceratitis cosyra: the role of temperature and resource pre‐emption. Entomologia Experimentalis et Applicata. 2009;133(1):27–37.
  63. 63. Wang H, Reitz SR, Xiang J, Smagghe G, Lei Z. Does temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS ONE. 2014;9(6):e98761. doi: 10.1371/journal.pone.0098761. pmid:24906119
  64. 64. Breeuwer A, Heijmans MM, Robroek BJ, Berendse F. The effect of temperature on growth and competition between Sphagnum species. Oecologia. 2008;156(1):155–67. doi: 10.1007/s00442-008-0963-8. pmid:18283501
  65. 65. Taniguchi Y, Rahel FJ, Novinger DC, Gerow KG. Temperature mediation of competitive interactions among three fish species that replace each other along longitudinal stream gradients. Can J Fish Aqua Sci. 1998;55(8):1894–901.
  66. 66. Taniguchi Y, Nakano S. Condition-specific competition: implications for the altitudinal distribution of stream fishes. Ecology. 2000;81(7):2027–39.
  67. 67. Carmona-Catot G, Magellan K, García-Berthou E. Temperature-specific competition between invasive mosquitofish and an endangered cyprinodontid fish. PLoS ONE. 2013;8(1):e54734. doi: 10.1371/journal.pone.0054734. pmid:23382951
  68. 68. Jiang L, Morin PJ. Temperature‐dependent interactions explain unexpected responses to environmental warming in communities of competitors. Journal of Animal Ecology. 2004;73(3):569–76.
  69. 69. Masters G, Brown V, Clarke I, Whitaker J, Hollier J. Direct and indirect effects of climate change on insect herbivores: Auchenorrhyncha (Homoptera). Ecological Entomology. 1998;23:45–52.
  70. 70. Jaramillo J, Muchugu E, Vega FE, Davis A, Borgemeister C, Chabi-Olaye A. Some like it hot: the influence and implications of climate change on coffee berry borer (Hypothenemus hampei) and coffee production in East Africa. PLoS ONE. 2011;6(9):e24528. doi: 10.1371/journal.pone.0024528. pmid:21935419
  71. 71. Scherber C, Gladbach DJ, Stevnbak K, Karsten RJ, Schmidt IK, Michelsen A, et al. Multi‐factor climate change effects on insect herbivore performance. Ecology and Evolution. 2013;3(6):1449–60. doi: 10.1002/ece3.564. pmid:23789058
  72. 72. Nooten SS, Andrew NR, Hughes L. Potential impacts of climate change on insect communities: a transplant experiment. PLoS ONE. 2014;9(1):e85987. doi: 10.1371/journal.pone.0085987. pmid:24465827
  73. 73. Kutywayo D, Chemura A, Kusena W, Chidoko P, Mahoya C. The impact of climate change on the potential distribution of agricultural pests: the case of the coffee white stem borer (Monochamus leuconotus P.) in Zimbabwe. PLoS ONE. 2013;8(8):e73432. doi: 10.1371/journal.pone.0073432. pmid:24014222
  74. 74. Rosenzweig C, Iglesias A, Yang X, Epstein PR, Chivian E. Climate change and extreme weather events; implications for food production, plant diseases, and pests. Global Change and Human Health. 2001;2(2):90–104.
  75. 75. Jaramillo J, Chabi-Olaye A, Kamonjo C, Jaramillo A, Vega FE, Poehling H-M, et al. Thermal tolerance of the coffee berry borer Hypothenemus hampei: predictions of climate change impact on a tropical insect pest. PLoS ONE. 2009;4(8):e6487. doi: 10.1371/journal.pone.0006487. pmid:19649255
  76. 76. Schoonhoven LM, Van Loon JJ, Dicke M. Insect-plant biology. Second ed: Oxford University Press; 2005. 421 p.
  77. 77. Kaufmann T. Behavioral biology, feeding habits, and ecology of three species of maize stem-borers: Eldana saccharina (Lepidoptera: Pyralidae), Sesamia calamistis and Busseola fusca (Noctuidae) in Ibadan, Nigeria, West Africa [Zea mays]. Journal of the Georgia Entomological Society. 1983;18:259–72.
  78. 78. Berger A. Ballooning activity of Chilo partellus larvae in relation to size of mother, egg batches, eggs and larvae and age of mother. Entomologia Experimentalis et Applicata. 1989;50(2):125–32.
  79. 79. Shanower T, Schulthess F, Bosque-Perez N. Development and fecundity of Sesamia calamistis (Lepidoptera: Noctuidae) and Eldana saccharina (Lepidoptera: Pyralidae). Bulletin of Entomological Research. 1993;83(02):237–43.
  80. 80. Van Rensburg J, Van Rensburg G, Giliomee J, Walters M. The influence of rainfall on the seasonal abundance and flight activity of the maize stalk borer, Busseola fusca in South Africa. South African Journal of Plant and Soil. 1987;4(4):183–7.
  81. 81. Matama-Kauma T, Kyamanywa S, Ogwang J, Omwega C, Willson H. Cereal stemborer species complex and establishment of Cotesia flavipes Cameron in eastern Uganda. International Journal of Tropical Insect Science. 2001;21(04):317–25.
  82. 82. Ndemah R, Schulthess F, Korie S, Borgemeister C, Poehling H- M, Cardwell K. Factors affecting infestations of the Stalk Borer Busseola fusca (Lepitoptera: Noctuidae) on maize in the forest zone of Cameroon with special reference to Scelionid Egg Parasitoids. Environmental Entomology. 2003;32(1):51–60.
  83. 83. Gounou S, Schulthess F. Spatial distribution of lepidopterous stem borers on indigenous host plants in West Africa and its implications for sampling schemes. African Entomology. 2004;12(2):171–8.
  84. 84. Jiang N, Zhou G, Overholt WA, Muchugu E, Schulthess F. The temporal correlation and spatial synchrony in the stemborer and parasitoid system of Coast Kenya with climate effects. Annales de la Société Entomologique de France. 2006;42(3–4):381–7.
  85. 85. Craig TP, Itami JK, Shantz C, Abrahamson WG, Horner J, Craig JV. The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis. Ecological Entomology. 2000;25(1):7–18.
  86. 86. De Moraes CM, Mescher MC, Tumlinson JH. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature. 2001;410(6828):577–80. pmid:11279494
  87. 87. Shiojiri K, Takabayashi J, Yano S, Takafuji A. Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecology Letters. 2002;5(2):186–92.