Developmental and reproductive performance of a specialist herbivore depend on seasonality of, and light conditions experienced by, the host plant

Osariyekemwen O. Uyi; Costas Zachariades; Lelethu U. Heshula; Martin P. Hill

doi:10.1371/journal.pone.0190700

Abstract

Host plant phenology (as influenced by seasonality) and light-mediated changes in the phenotypic and phytochemical properties of leaves have been hypothesised to equivocally influence insect herbivore performance. Here, we examined the effects of seasonality, through host plant phenology (late growth-season = autumn vs flowering-season = winter) and light environment (shade vs full-sun habitat) on the leaf characteristics of the invasive alien plant, Chromolaena odorata. In addition, the performance of a specialist folivore, Pareuchaetes insulata, feeding on leaves obtained from both shaded and full-sun habitats during autumn and winter, was evaluated over two generations. Foliar nitrogen and magnesium contents were generally higher in shaded plants with much higher levels during winter. Leaf water content was higher in shaded and in autumn plants. Total non-structural carbohydrate (TNC) and phosphorus contents did not differ as a function of season, but were higher in shaded foliage compared to full-sun leaves. Leaf toughness was noticeably higher on plants growing in full-sun during winter. With the exception of shaded leaves in autumn that supported the best performance [fastest development, heaviest pupal mass, and highest growth rate and Host Suitability Index (HSI) score], full-sun foliage in autumn surprisingly also supported an improved performance of the moth compared to shaded or full-sun leaves in winter. Our findings suggest that shaded and autumn foliage are nutritionally more suitable for the growth and reproduction of P. insulata. However, the heavier pupal mass, increased number of eggs and higher HSI score in individuals that fed on full-sun foliage in autumn compared to their counterparts that fed on shaded or full-sun foliage in winter suggest that full-sun foliage during autumn is also a suitable food source for larvae of the moth. In sum, our study demonstrates that seasonal and light-modulated changes in leaf characteristics can affect insect folivore performance in ways that are not linear.

Citation: Uyi OO, Zachariades C, Heshula LU, Hill MP (2018) Developmental and reproductive performance of a specialist herbivore depend on seasonality of, and light conditions experienced by, the host plant. PLoS ONE 13(1): e0190700. https://doi.org/10.1371/journal.pone.0190700

Editor: Gadi V. P. Reddy, Montana State University Bozeman, UNITED STATES

Received: September 22, 2017; Accepted: December 19, 2017; Published: January 5, 2018

Copyright: © 2018 Uyi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper.

Funding: The authors thank the Department of Environmental Affairs: Natural Resource Management Programmes and ARC-Plant Protection Research Institute, South Africa for providing funding and facilities. The first author wishes to thank the German Academic Exchange Service (DAAD) for funding his PhD studies and The World Academy of Sciences (TWAS), and the National Research Foundation (NRF) of South Africa for funding his postdoctoral research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Competing interests: The authors have declared that no competing interests exist.

Introduction

Decades of studies have established the importance of host plant quality, including foliar nutrients, for herbivore performance (e.g. survival, growth and reproduction) and population dynamics [1–4]. Foliage quality is known to be influenced by a multiplicity of environmental factors such as seasonality (through its effects on host plant phenology) and light conditions [5–8]. From the viewpoint of nutritional ecology, the response of insect herbivores (in terms of survival, growth and reproduction) to independent and combined effects of seasonality and light conditions on the foliar quality of their host plants remains equivocal despite several studies [8–12]. Therefore, advancing our understanding of the relationship between foliage quality and phytophagous insect performance, and how abiotic conditions (e.g. seasonality, light conditions) singly, or in combination, influence this relationship is central to our knowledge of the nutritional ecology of insects and the evolution of their life histories.

The physiology, anatomy, phytochemistry of, and biochemical processes in individuals of the same plant species often vary according to host plant phenology due to seasonality. These variations are known to affect the nutritional quality of leaves by altering their physical and chemical characteristics such as leaf toughness, foliar nitrogen, water, phosphorus and carbohydrate contents as well as the concentrations of secondary chemicals [5–7, 9, 13]. For example, the concentration of foliar nitrogen, which is thought to be the most limiting macronutrient for insect herbivores, in trees and shrubs, is known to be higher during winter (and lower in autumn or summer) due to the plant’s biochemical response to low temperatures [13, 14]. Consequently, seasonal variation in foliar quality has been reported to influence the behaviour, performance, abundance and population density of insect herbivores [15, 16] and has been implicated (along with temperature) in insect population outbreaks [17].

In nature, individuals of the same species growing in different light environments (e.g. shaded vs full-sun habitats) often exhibit a degree of phenotypic and phytochemical variation [12, 18, 19] primarily because light intensity directly influences the physiological, growth and biochemical processes in plants by directly controlling carbon intake through photosynthesis [13, 20, 21]. The carbon/nutrient balance (C/NB) hypothesis [22, 23, 24] postulates that leaves of plants growing under sub-optimal levels of photosynthetically active radiation (e.g. in shaded habitat) should contain relatively more mineral nutrients, especially nitrogen and relatively less carbon-based secondary (defence) compounds (e.g. phenolics, tannins) compared to plants growing in full-sun environment. Leaves of plants growing in low light environments are often carbon limited and have been observed to exhibit reduced total non-structural carbohydrate (TNC) [12], increased foliar nitrogen [8, 18, 25, 26] and water content [8] as well as reduced tannins and phenolics [12], predicting that leaves of shaded plants should be better food for herbivorous insects. These light-mediated changes in the foliage quality of host plants have been demonstrated to influence insect herbivore performance in ways that are not straightforward [8, 12, 16, 18, 27], as evident in studies testing the C/NB hypothesis in this context [11, 28].

Despite reports that seasonality or plant phenology and light intensity alter plant quality and consequently indirectly affect insect performance, studies that explicitly or simultaneously assessed the relative roles of the indirect influence of both factors on host plant quality and on herbivores performance (through their effects on foliage quality) are scarce [6, 16]. If habitat heterogeneity due to sunlight conditions and temporal patterns of variation interact (e.g. some areas that are shaded in summer could become sunny in winter), leaves of individual plants of the same species in different habitats may be favourable for herbivores at different points in time. Such spatio-temporal variation would not only create temporally variable patterns of insect distribution and abundance [29], but may also influence the developmental and reproductive performance in phytophagous insects such as Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae), a specialist folivore that was introduced from Florida, USA, into South Africa, for the biological control of the invasive alien plant, Chromolaena odorata (L.) King and Robinson (Asteraceae). Understanding how P. insulata responds to seasonal and spatial variations in the quality of its host plant will not only advance our knowledge of the nutritional ecology of this multivoltine moth, but may also help to explain its usually low population levels in the field in South Africa.

Previous studies, including ours, that evaluate the performance of insect herbivores on foliage from full-sun versus shaded environments, infrequently consider seasonality and host plant phenology or conduct such investigations at only one point in time [8, 18, 19]. The phenology of C. odorata is seasonal, with the flowering of mature plants in winter (between June and August) in the southern hemisphere. To our knowledge, the combined effects of seasonality (through its effects on host plant phenology) and light intensity on the leaf characteristics of C. odorata are unknown. Most importantly, it is not known whether the performance of the moth on shaded versus full-sun leaves varies according to season or host plant phenology. Here, we examined the effects of host plant phenology as influenced by seasonality (late growth-season = late summer/autumn and flowering-season = winter/early spring) and light conditions (shaded and full-sun) on the physical and chemical characteristics of C. odorata plants in order to determine the concentrations of the various potentially important nutrients in C. odorata plants in the different microhabitats and seasons. For purposes of convenience, the late summer/autumn trial will be called the ‘autumn trial’ and the winter/early spring trial will be called the ‘winter trial’ from here on. A further objective of this study was to determine whether seasonal and light-mediated changes in the phenotypic and phytochemical properties of C. odorata influence the performance of P. insulata by evaluating the survival, growth and reproductive metrics of the moth, by feeding the larvae on leaves obtained from both shaded and full-sun habitats during autumn and winter. We predicted that the physical and chemical characteristics of C. odorata leaves would be influenced by seasonality, and that the leaves of shaded plants would be of better quality for development and reproduction of P. insulata compared to full-sun ones, as proposed by the carbon/nutrient balance hypothesis. We also predicted that seasonal- and sunlight-mediated changes in the leaf characteristics of C. odorata plants will interactively influence the developmental and reproductive performance of P. insulata.

Materials and methods

Study organisms

Chromolaena odorata is perennial pioneering shrub that is native to the Americas (from southern USA to northern Argentina, including the Caribbean islands), but is now widespread in parts of Africa, Asia and Oceania, where it impacts negatively on agriculture, conservation of biodiversity, eco-tourism and livelihoods [30, 31]. The biotype of C. odorata that has invaded southern Africa, which originated from Cuba or Jamaica, is morphologically and genetically different from the more widespread biotype (Asia/West African biotype) invading Asia, Oceania, West, East and Central Africa [32]. Our study utilised the southern African biotype. In a high-light environment or in open situations, the shrub can grow up to 2–3 metres in height, but it can reach up to 5–10 metres when supported by other vegetation in semi-shaded habitats [30]. In South Africa, prolific flowering occurs during winter in June and July after the cessation of vegetative growth.

Pareuchaetes insulata is a multivoltine specialist herbivore that is native to the Americas (from southern USA to north-western South America), and was introduced into South Africa between 2001 and 2009 for the biological control of C. odorata. Under laboratory conditions and in field outbreak situations, the larvae of this moth can extensively defoliate C. odorata. The biology of this golden yellow moth is documented in Kluge and Caldwell [33] and Uyi et al. [34]. Following the release of over 1.9 million individuals of different life stages of P. insulata (from Florida—USA, Cuba and Jamaica), only the Floridian population (880,000 individuals of different life stages) is considered to have established after it was released at some 21 sites in KwaZulu-Natal (KZN) province, South Africa. It is unknown if populations from Cuba and Jamaica may have interbred with it and provided genetic material to the current population [35]. Although this insect did establish, its population levels are generally low in the field, albeit with occasional outbreaks and a degree of impact on the weed [36]. The variable performance and low population levels of the moth make it a difficult candidate to study in a field situation.

Measurement of physical and chemical characteristics of leaves

Leaf characteristics of C. odorata plants growing in fields within the vicinity of the South African Sugarcane Research Institute (SASRI), Mount Edgecombe (29° 70’ S, 31° 05’ E), near Durban, South Africa, were studied. The South African Sugarcane Research Institute granted us permission to use their field sites and facilities. The field chosen consisted of full-sun (or open) and shaded habitats and measured 0.7 hectares. Three years (2010–2012) of annual weather data obtained from the South African Weather Service showed that the average daily temperature in the closest weather station [King Shaka International Airport (29° 36’ S, 31° 06’ E), Durban, South Africa] to the study site ranged between 11.2 and 28.9°C, and annual rainfall ranged between 870.5 and 1052.8 mm. The full-sun habitat was fully exposed to sunlight and was dominated by C. odorata, with a sparse population of Lantana camara L. (Verbenaceae), while the shaded habitat was partially exposed to sunlight and consisted of trees of Syzygium guineense (Wild.) DC. (Myrtaceae) and bugweed, Solanum mauritianum Scop. (Solanaceae). Light intensity (measured by a light meter, LX–101, Taiwan) differed significantly between the two habitats in autumn (mean ± SE: 1872.17 ± 23.36 and 347.21 ± 20.22 lux for full-sun and shaded habitat respectively; GLM ANOVA, F_1,19 = 2436.82, P < 0.0001) and winter (mean ± SE: 1882.10 ± 34.251 and 358.23 ± 14.87 lux for full-sun and shaded habitat respectively; GLM ANOVA, F_1,19 = 921.243, P < 0.0001) (see Uyi et al. [19] for further details about the study site). The leaf characteristics and insect performance study were conducted in winter/early spring 2013 (from July 15^th to October 6^th, 2013 = winter trial) and late summer/autumn 2014 (from March 11^th to June 4^th, 2014 = autumn trial) as a comparison, while the larval preference trial was conducted in early winter 2017 (6-8^th June 2017). All plants used in the winter trials were at the flowering and seeding stage whereas the ones used in the autumn trials were nearing the end of their vegetative growth season, and had not started flowering. It is possible that there might be a difference in the chemistry / nutrient allocation of flowering versus seeding plants. In C. odorata, the initiation of flowering in winter causes all further production of new leaves to cease. One of the reasons why we chose late autumn plants as opposed to spring plants plants for this study is because all occasional outbreaks of the moth usually occur during this period [36].

The specific leaf weight (SLW), which provides a physiological estimate of ‘leaf toughness’ [37] of 100 fully expanded leaves (taken from the upper half of the plants) obtained from 20 plants per habitat type (5 leaves per plant) in August 2013 (winter) and April 2014 (autumn) was estimated in both shaded and full-sun habitats following the methods described in our earlier study [19]. Different 20 plants were sampled in August 2013 and April 2014. To determine whether seasonality and habitat conditions influence the foliar chemistry of C. odorata plants, leaf materials collected from 10 randomly selected C. odorata plants along a 20 m transect in each habitat in both autumn and winter were subjected to analyses at the laboratories of the Fertilizer Advisory Service, SASRI and KZN Department of Agriculture and Rural Development, South Africa. Following measurement of the wet weight of the leaf materials, they were dried for 72 h at 65°C and N and C contents were determined as a percentage of dry weight using a TruSpec^® CN analyser (LECO, St Joseph, MI, USA). After ashing of a subsample, P was determined colorimetrically [38], and K, Ca, and Mg using atomic absorption spectrophotometry. The amount of the total non-structural carbohydrate (TNC) in leaves was analysed using the acid hydrolysis procedure [39]. Finally, the acid detergent lignin content was analysed using the methods described in van Soest [40], while water content (%) was calculated using the formula: [(leaf fresh weight–leaf dry weight) / leaf fresh weight] × 100%.

Development and reproductive performance of Pareuchaetes insulata

For the winter trial, the larvae used in the insect performance experiments were obtained from eggs laid by F₁ adult females whose original parents were collected in May 2013 on light traps at the Sappi Cannonbrae plantation, Umkomaas (30^o 13’ S, 30^o 46’ E) (south coast of KZN province), South Africa. For the autumn trial, the larvae used in the insect performance experiments were obtained from eggs laid by F₁ adult females whose original parents were collected in February 2014 on light traps at the same location as above. The parents (males and females) were placed in aerated 700 ml plastic containers, each with a 5 cm diameter mesh window at the top, with C. odorata stem cuttings plugged into a moistened Oasis^TM floral foam block (5 × 5 × 3 cm) wrapped with aluminium foil for egg laying. They were provided with a cotton-wool ball soaked with a 50% (wt/vol) honey solution and kept in the laboratory (25 ± 2 ^oC, 65 ± 10% relative humidity (RH), L12:D12) at the Weeds Biocontrol Research Laboratory of the ARC-Plant Protection Research Institute (ARC-PPRI), KZN, South Africa (29° 32’ S, 30° 16’ E). Hatched larvae (from eggs laid) were fed on leaf cuttings obtained from plants in 25 cm-diameter pots (see Uyi et al. [41] for details of the potting medium). The resulting adults (1 virgin female and 2 newly eclosed males) were placed in 700 ml containers as described above. The eggs laid by these females were used for this study.

The performance experiments were conducted in a temperature-controlled room maintained at 25°C, 68% RH and 12D:12L photoperiod at SASRI. Hygrochron iButtons (model DS 1923, Maxim Integrated Products, San José, USA, 0.5°C accuracy) were used to measure temperature and RH at hourly intervals during winter (temperature range, 23.69 to 26.19 ^oC; mean ± SE, 24.84 ± 0.01 ^oC; RH range, 66.5 to 75.3%; mean ± SE, 70.51 ± 2.13%) and autumn (temperature range, 24.45 to 26.74 ^oC; mean ± SE, 24.95 ± 0.01 ^oC; RH range, 68.4 to 78.1%; mean ± SE, 71.34 ± 2.16%). For both the winter and autumn study, newly hatched (unfed) F₁ larvae were placed individually, using a fine brush, into transparent 100 ml aerated plastic containers (one larva per container), each with a circular screen window of 2.5 cm diameter at the top, lined at the bottom with moistened filter paper to maintain RH, and fed on C. odorata foliage (fully expanded leaves taken from the upper half of plants in the field) obtained from either shaded or full-sun habitat. All leaf materials were obtained fresh from over eight plants per habitat on each collection date (every 48 h) at the field site and replaced by new materials from different plants every 48 h. One hundred replicates (= 100 larvae) were used for each foliage type. In this way, a total of 400 individuals (100 per foliage type in autumn and winter trials) of P. insulata were studied for two successive generations. Therefore 800 larvae were studied. The autumn and winter trials were conducted using Completely Randomized Design (CRD). Leaf materials were replaced every 48 hours and frass was removed at same interval for hygienic reasons [42]. The larvae were monitored daily until pupation and/or adult eclosion in order to record mortality and follow the duration of larval instars and the pupal stage. The following variables were measured or recorded for both shaded and full-sun foliage-fed individuals in both seasons: (1) total immature development time (duration from egg hatch to adult eclosion), (2) pupal mass, and (3) growth rate [pupal mass (mg) / development time]. We also calculated Maw’s host suitability index (HSI) using the following equation: HSI = (female pupal mass × % pupation) / immature development time (for rationale, see Maw [43]). Newly hatched larvae (F₂ or their progeny) resulting from F₁ adults in this experiment were also subjected to similar treatment as described above (for the larval performance trial). Two generations of the insect were studied, because only two generations of this insect can be obtained within a particular season.

When the adults of both the “parental generation” (F₁) and progeny (F₂) eclosed, 1 virgin female and 2 newly eclosed males that had fed on either shaded or full-sun foliage as larvae were placed in 700 ml containers as described above (as was done for oviposition of field-collected adults) but they were provided with stem cuttings (with leaves) of the plant type (shaded and full sun) they had fed on as larvae. Previous studies suggest that night-active species do not discriminate (for oviposition) between foliage in the sun or shade as the proximal light micro-environment encountered by the ovipositing females do not differ at night [44]. Therefore, we maintained all experimental containers under the same light condition, (L12:D12). During the winter trials, 43 replicates each were used for full-sun and shaded habitat trials (86 in total), while during the autumn trials, 34 and 35 replicates (69 in total) were respectively used for full-sun and shaded habitat trials. The containers and leaves were examined daily to record the following: (i) adult longevity and (ii) numbers of eggs laid.

Larval preference test

To test the attractiveness of full-sun and shaded foliage of C. odorata to P. insulata, freshly collected young, fully expanded leaves of each of these two foliage types were used following the methods described in Uyi et al. [41]. Rectangular pieces of leaf tissue (20 × 40 mm) were placed in 140-mm-diameter Petri dishes containing a 90-mm-diameter disc of filter paper moistened with 0.6 ml of water. Two rectangles of leaf tissue from shaded C. odorata foliage were placed alternately around the edge of the Petri dish with those of full-sun and 20 unfed neonate P. insulata were placed haphazardly (but not on the leaves) using a fine brush in each Petri dish. Twenty replicates were used per foliage type and the leaf tissues used were taken from 40 different plants. Following a 24 hour treatment, each dish was opened and the number of larvae on each leaf piece was counted.

Statistical analysis

The effect of season (plant phenology: late growth-season vs flowering-season plants) and habitat condition on leaf characteristics were evaluated using univariate General Linear Model analysis of variance (GLM ANOVA). When the overall results were significant in a two-way analysis, the differences among the treatments were compared using the Tukey’s HSD test because of the equality of sample sizes. We performed statistical analyses based only on the number of individual larvae that successfully eclosed as adults. Data from pupae that failed to eclosed were discarded because we wanted to be sure that handling (disturbance) during measurement (= weighing) did not negatively affect adult eclosion success. Data from two successive generations per habitat type within each season were combined and used for the analyses of insect performance metrics to allow for a more robust analysis. Pearson’s χ² test was used to compare the effect of season and habitat condition on total immature survival. The effect of season (autumn vs winter) and habitat condition (shade vs full-sun) on total development duration, pupal mass, growth rate, host suitability index (HSI), number of eggs laid and adult longevity were evaluated using GLM ANOVA. When the overall results were significant, the differences among the treatments were compared using Tukey-Kramer’s test. The percentage preference for foliage type by neonate larvae was evaluated using student’s t test With the exception of the GLM ANOVA that was performed using SPSS Statistical software, version 16.0 (SPSS, Chicago, USA), all other analysis were performed using Genstat 14.0 (VSN International, Hemel Hempstead, UK).

Results

Leaf characteristics

Results indicated that seasonality and habitat conditions independently and interactively impacted foliar nitrogen content of C. odorata plants. Foliar nitrogen concentration was 69.2% and 52.5% higher in shaded plants (relative to full-sun plants) for winter and autumn, respectively (Table 1; Fig 1A). Foliar nitrogen concentration was 18.6% higher in winter compared to autumn in the shaded habitat, but its concentration in the full-sun habitat did not differ between winter and autumn plants. Phosphorus concentration was slightly higher in the full-sun habitat in both autumn and winter (Table 1; Fig 1B). The calcium concentration did not differ between seasons or between habitats (Table 1; Fig 1C). Although magnesium concentration was higher in shaded habitat in winter, it did not differ between habitats in autumn (Table 1; Fig 1D). The concentration of potassium was higher in autumn than winter and the shaded habitat had significantly higher concentration compared to full-sun habitat (Table 1; Fig 1E). Lignin content did not differ between seasons, but was statistically higher in shaded habitats in both autumn (13.11%) and winter (13.72%) (Table 1; Fig 1F). Although the concentration of total non-structural carbohydrate (TNC) did not vary between autumn and winter, it was 64.3 and 50.0% higher in the full-sun habitat in winter and autumn respectively (Table 1; Fig 1G) compared to the shaded habitat. Leaf water content was higher for plants growing in the shaded habitat in both autumn and winter and was higher in autumn compared to winter (Table 1, Fig 1H). Specific leaf weight (SLW, an indication of leaf toughness) was influenced by seasonality (or host plant phenology), habitat condition and their interaction (Table 1, Fig 2). Leaf toughness in the full-sun habitat was 97.35% greater than that in the shaded plants in winter and 54.28% greater than shaded habitat in autumn (Table 1, Fig 2).

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Fig 1. Seasonal (autumn vs winter) variation in the phytochemistry (including nutrients, % dry mass) of the leaves of Chromolaena odorata plants in two habitats (shade vs full sun).

Data represent means ± SE. Bars within each graph not sharing a common letter differ significantly (P < 0.05) after Tukey’s Honest Significant Difference (HSD) test.

https://doi.org/10.1371/journal.pone.0190700.g001

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Fig 2. Seasonal (autumn vs winter) variation in leaf toughness [as indicated by specific leaf weight (SLW)] of Chromolaena odorata plants in two habitats (shade vs full sun).

Data represent means ± SE. Bars within each graph not sharing a common letter differ significantly (P < 0.05) after Tukey’s Honest Significant Difference (HSD) test.

https://doi.org/10.1371/journal.pone.0190700.g002

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Table 1. Statistical details (GLM ANOVA) for the analyses of the effects of season (autumn vs winter) and habitat condition (shade vs full-sun) on physical and chemical characteristics of Chromolaena odorata leaves.

https://doi.org/10.1371/journal.pone.0190700.t001

Developmental and reproductive performance of Pareuchaetes insulata

Overall, immature survival of P. insulata (first instar to adult eclosion) was influenced by seasonality (Pearson χ² = 5.17, d.f. = 1, P = 0.023), with autumn foliage supporting higher survival compared to winter foliage (Fig 3). However, no significant difference in immature survival due to foliage types was detected (Pearson χ² = 0.28, d.f. = 1, P = 0.599) (Fig 3). Total development time, pupal mass, growth rate, host suitability index (HSI) and fecundity were influenced by seasonality (or host plant phenology), habitat condition, and their interactions (Table 2; Figs 4A–4D and 5A). Total development was significantly faster on shaded leaves in both autumn and winter (Fig 4A). Although faster development time was evident in autumn compared to winter irrespective of habitats, it was similar between individuals that fed on shaded leaves in winter and those that fed on full-sun leaves in autumn. Generally, autumn foliage supported heavier pupal mass compared to winter ones (Fig 4B). Pupal mass was evidently heavier in individuals that fed on shaded leaves in winter compared to those that fed on full-sun foliage in the same season, but this variable did not differ between foliage types in autumn (Fig 4B). Individuals reared on autumn foliage had a higher growth rate than those that were fed on winter foliage (Fig 4C). Irrespective of season or host plant phenology, growth rate was always higher in individuals fed on shaded leaves compared to those that fed on full-sun leaves (Fig 4C). Larvae fed on shaded or autumn leaves had higher Maw’s HSI values (Fig 4D).

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Fig 3. Seasonal (autumn vs winter) variation in percentage survival (mean ± SE) of combined immature stages of Pareuchaetes insulata reared on Chromolaena odorata leaves from two different habitats (shade vs full sun).

Bars with different letters are significantly different (Pearson χ²; P < 0.05). Each bar represents percentage survival out of 400 first instar larvae monitored until adult eclosion.

https://doi.org/10.1371/journal.pone.0190700.g003

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Fig 4.

Seasonal (autumn vs winter) variation in total development duration (a), pupal mass (b) growth rate (c) and host suitability index (d) of Pareuchaetes insulata reared on Chromolaena odorata leaves from two different habitats. Data represent means ± SE. Bars within each graph not sharing a common letter differ significantly (P < 0.05) after Tukey-Kramer test.

https://doi.org/10.1371/journal.pone.0190700.g004

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Fig 5.

Seasonal (autumn vs winter) variation in mean number of eggs (a) and mean adult longevity (b) of Pareuchaetes insulata reared on Chromolaena odorata leaves from two different habitats (shade vs full sun). Data represent means ± SE. Bars within each graph not sharing a common letter differ significantly (P < 0.05) after Tukey-Kramer test.

https://doi.org/10.1371/journal.pone.0190700.g005

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Table 2. Statistical details (GLM ANOVA) for the analyses of the effects of season (autumn vs winter) and habitat condition (larval food source) on total development duration, pupal mass, growth rate, host suitability index, number of eggs and adult longevity.

https://doi.org/10.1371/journal.pone.0190700.t002

Generally, autumn foliage supported higher number of eggs compared to winter foliage (Fig 5A). Number of eggs was evidently higher in females that fed on shaded leaves (as larvae) in winter compared to those that fed on full-sun foliage in the same season, but this variable did not vary between foliage types in autumn. Adult longevity did not differ as a function of foliage type in winter, but varied between habitats in autumn–with individuals that fed on full-sun foliage living slightly longer than their counterparts that were reared on shaded leaves (Table 2, Fig 5B). Interestingly, individuals that fed on full-sun foliage in autumn had heavier pupal mass, increased number of eggs and higher HSI score compared to their counterparts that fed on shaded or full-sun foliage in winter.

Larval preference

Neonate larvae (newly emerged larvae) of P. insulata did not display any distinguishable preference for, or attractiveness to either shaded or full-sun foliage (mean ± SE, full-sun: 51.33 ± 3.09; shade: 48.67 ± 3.07; t₁,₃₈ = 0.61, P = 0.546).

Discussion

The higher concentration of foliar nitrogen in shaded plants in winter has not been previously reported in C. odorata, however, it has been shown in several plant species that foliar nitrogen increases in winter compared to summer or autumn [13, 45, 46]. The seasonal variation in leaf nitrogen suggests that the plants alter their nitrogen concentration to maximize daily nitrogen-use efficiency of carbon gain in response to varying seasonal temperatures, as has been reported by other workers [13]. The lower leaf water content and the increased leaf toughness in winter (relative to autumn) might be due to the seasonally dry winter (low winter rainfall) in areas invaded by C. odorata in South Africa. The presence of significant interactions in foliar nitrogen content and leaf toughness between light conditions and seasonality suggests that the effect of light condition was more apparent or stronger in winter compared to autumn. As predicted by the carbon nutrient balance (C/NB) hypothesis [22, 23, 24], leaves of C. odorata plants growing under sub-optimal levels of photosynthetically active radiation (= shaded plants) had relatively more mineral nutrients (e.g. increased nitrogen, magnesium, potassium and water contents) and reduced leaf toughness. The reduced leaf nitrogen and water as well as the increased concentration of TNC and leaf toughness in leaves of plants growing in full-sun concurs with the findings for other plant species [12, 18, 47], although a few studies have reported the opposite pattern [27]. The ostensibly higher lignin content in shaded habitat in both seasons might seem incongruous, however, it is consistent with the findings of Onoda et al. [48] who found that shaded leaves also had higher acid detergent fibre (ADF, such as lignin) concentration per unit mass. Although phosphorus, magnesium and potassium are important in several processes in plant growth and development, their role in C. odorata plants and the reason why they seasonally or phenologically and spatially vary in C. odorata leaves are unknown. The above results are consistent with our prediction that seasonality and light condition can alter the leaf characteristics of C. odorata plants. The changes in the plant characteristics due to the single, combined or interactive effects of both factors can influence the preference and performance of insect herbivores–and perhaps advance our fundamental understanding of insect plant interactions.

In this study, we observed that seasonal (or phenological) and light mediated changes in the phenotypic and phytochemical properties of C. odorata singly or interactively influenced the performance of P. insulata. For instance, development was faster, growth rate was higher, pupal mass was heavier and increased number eggs was noticeably evident in individuals that fed on shaded (relative to full-sun) or autumn (relative to winter) foliage. However neonate larvae did not display a preference for either shaded or full-sun foliage in this study. Pupal mass and development time are the most frequently used indicators that show how insects respond to their host’s nutritional quality and perhaps may predict changes to other important aspects of insect biology such as survival, behaviour, physiology and fecundity [49, 50]. A reduction in larval or pupal weight is generally known to affect future reproductive success by reducing adult body size, and possibly fecundity [34, 51]. Prolonging development time negatively affects the survival of immature stages (in a field situation) by exposing them to possible predation, parasitism, or unfavourable environmental conditions for a longer period [49, 52].

The spatial and temporal variation in the leaf characteristics of the plants can help explain the apparent superiority of shaded and autumn foliage. For instance foliar nitrogen was 69.2 and 52.5% higher in shaded plants (relative to full-sun) in both winter and autumn respectively. Increased foliar nitrogen has been linked to faster development time, higher survival rate, increased body mass, high growth rates and increased fecundity and population density in erebid moths and other insect species [1, 8, 53]. The prolonged development time, decreased pupal mass and growth rate as well as the reduced number of eggs in individuals that fed on shaded leaves in winter (when foliar nitrogen was 18% higher than autumn) relative to those that fed on shaded leaves in autumn, indicates that increased nitrogen levels in winter might have imposed a constraint on herbivore physiology. This finding supports theoretical predictions that insect herbivore performance increases with nutrient levels, but then plateaus due to diminishing returns or even declines at higher nutrient levels due to nutrient toxicity [4, 54]. The increased water content in shaded (relative to full-sun) and autumn (relative to winter) leaves as well as the reduced leaf toughness of shaded foliage in both seasons might have contributed to the faster development time, higher growth rate and increased pupal mass in P. insulata, as decreased leaf toughness and increased leaf water content are often linked to improved herbivore performance [18], although other authors [11, 12] have reported equivocal patterns. The better performance of P. insulata in autumn, correlated with a slight increase in foliar phosphorus content. The importance of dietary phosphorus on the survival, growth and development of some insects have been documented [53], but its relevance in the performance of P. insulata remains a question that needs to be investigated further. An increase in potassium and a decrease in magnesium in autumn coincided with improved performance of P. insulata in this study. Although very little is known about how variations in potassium and magnesium concentrations can affect insect herbivores, the concentrations of both elements are known to be positively associated with insect population density [55]. The lack of significant differences in pupal mass and number of eggs between individuals that fed on shaded and full-sun leaves in autumn suggests that leaf nutrients were more suitable for the herbivore than in winter. The improved performance of P. insulata on shaded foliage in both seasons supports the predictions of the C/NB hypothesis. However, the better performance of individuals of the moth on full-sun foliage in autumn compared to their counterparts that were reared on shaded or full-sun foliage in winter does not appear to extinguish the debates surrounding the C/NB hypothesis in terms of herbivore performance.

The better performance of the moth on full-sun leaves in autumn relative to full-sun or shade leaves in winter suggests that full-sun foliage growing in autumn are a suitable source of food in the absence of shaded plants. This is surprising because many studies often report improved performance of insect herbivores on shaded foliage [15, 18]. If we had not conducted studies across a seasonal spectrum (autumn vs winter), we wouldn’t have been able to detect this. The improved overall performance of the moth on autumn foliage (relative to winter) further suggests that autumn foliage satisfied the nutritional requirements of the insect possibly due to increased rainfall and or temperature during this period. Even though the population remained low in the field, our study allows us to hypothesize that P. insulata should be more abundant during autumn months because of the better quality of leaves during this period. Our results further suggest that C. odorata growing in shaded habitats or in full-sun habitats in autumn, may enhance the establishment and/or performance of biological control agents such as Pareuchaetes species.

Outside the indirect effects of seasonality (low winter temperature: through host plant phenology and quality) on herbivore performance (in this study), recent studies suggest that direct and indirect effects of low winter temperatures can reduce the mobility, prolong development time and compromise other life history events or traits in P. insulata [56, 57]. A combination of both direct and indirect effects of low winter temperatures (through direct effects and through host plant quality) may represent a double-blow for the insect during winter months, or in cold areas, and this may subsequently be detrimental for the populations of this insect in the field, particularly given its native-range climate.

Whatever specific nutritional attributes ultimately determine plant quality per se in this study, is far from being the only factor affecting insect fitness. The importance of, for instance, secondary chemicals (see reviews in [58, 59]) and natural enemies [60] has been proven beyond doubt, and to complicate matters further, these factors may interact with plant quality as determinants of insect herbivore performance and population density. The concentration of the secondary chemical, pyrrolizidine alkaloids (PAs) in other arctiine moths such as Utetheisa ornatrix (L.) (Lepidoptera: Erebidae) is known to play a key role in the mating biology and in the defence of immature stages against predators and parasitoids [58, 61]. For example, smaller adult males have less chance of mating [62], and if mating does occur, parent females may produce small-sized offspring resulting in reduced adult fecundity, and compromising the fitness of immature stages–as smaller-sized adults are likely to produce eggs with reduced PAs [58]. Whether secondary chemicals (including PAs) in C. odorata vary with seasonality, plant phenology and light intensity, and whether these variations would influence P. insulata performance still remains a question. While herbivorous insects from families with exposed larvae (such as P. insulata) are unlikely to be heavily parasitized in a new geographical range [60, 63], the role of predators on the different life stages of P. insulata needs further investigation across a spatio-temporal spectrum.

To conclude, this study demonstrated that seasonality (through its effect on host plant phenology) and light environment contributes to altered leaf chemistry (e.g. nitrogen, magnesium, phosphorus and TNC), leaf physiology (leaf water content) and leaf defence (leaf toughness) of C. odorata plants and that these variability consequently influenced the developmental and reproductive performance of P. insulata in ways that are not straightforward. These findings are largely consistent with our earlier predictions (see introduction). To our knowledge, the current study is the first to report how seasonal and light mediated variability in host plant influence herbivore performance in the bitrophic interaction between C. odorata and any arctiine moth, but whether or not it extends to other species in the broader field of light environment-effects on herbivore-host plant interactions is unknown, and requires further studies on other systems.

Acknowledgments

We are grateful to the South African Sugarcane Research Institute, Mount Edgecombe, near Durban, South Africa, for granting us access to use their facilities. The South African Weather Service is thanked for providing climate data.

References

1. Myers JH, Post BJ. Plant nitrogen and fluctuations of insect populations: a test with the cinnabar moth-tansy ragwort system. Oecologia. 1981; 48: 151–156. pmid:28309793
- View Article
- PubMed/NCBI
- Google Scholar
2. Awmack CS, Leather SR. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology. 2002; 47: 817–844. pmid:11729092
- View Article
- PubMed/NCBI
- Google Scholar
3. Uyi OO, Zachariades C, Hill MP. Nitrogen fertilization improves growth of Chromolaena odorata (Asteraceae) and the performance of the biological control agent, Pareuchaetes insulata (Erebidae). Biocontrol Science and Technology. 2016; 26: 373–385.
- View Article
- Google Scholar
4. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R. Variability in plant nutrients reduces insect herbivore performance growth and mortality. Nature. 2016; 539(7629): 425–427. pmid:27749815
- View Article
- PubMed/NCBI
- Google Scholar
5. Osier TL, Jennings SM. Variability in host plant quality for the larvae of a polyphagous insect folivore in midseason: the impact of light on three deciduous sapling species. Entomologia Experimentalis et Applicata. 2007; 123: 159–166.
- View Article
- Google Scholar
6. Karolewski P, Giertych MJ, Żmuda M, Jagodziński AM, Oleksyn J. Season and light affect constitutive defenses of understory shrub species against folivorous insects. Acta Oecologica. 2013; 53: 19–32.
- View Article
- Google Scholar
7. Carvalho S, Macel M, Mulder PPJ, Skidmore A, van der Putten WH. Chemical variation in Jacobaea vulgaris is influenced by the interaction of season and vegetation successional stage. Phytochemistry. 2014; 99: 86–94. pmid:24412324
- View Article
- PubMed/NCBI
- Google Scholar
8. Uyi OO, Uwagiahanor BI, Ejomah AJ. The nocturnal larvae of a specialist folivore prefer Chromolaena odorata (L.) foliage from a sunny environment, but does it matter? Arthropod-Plant Interactions. 2017; 11: 603–611.
- View Article
- Google Scholar
9. Alonso C, Herrera CM. Seasonal variation in leaf characteristics and food selection by larval noctuids on an evergreen Mediterranean shrub. Acta Oecologica. 2000; 21: 257–265.
- View Article
- Google Scholar
10. Gripenberg S, Salminen J, Roslin T A tree in the eyes of a moth—temporal variation in oak leaf quality and leaf-miner performance. Oikos. 2007; 116: 592–600.
- View Article
- Google Scholar
11. Sarfraz RM, Kharouba HM, Myers JH. Tent caterpillars are robust to variation in leaf phenology and quality in two thermal environments. Bulletin of Entomological Research. 2013; 103: 522–529. pmid:23464617
- View Article
- PubMed/NCBI
- Google Scholar
12. Łukowski A, Giertych MJ, Zadworny M, Mucha J, Karolewski P. Preferential feeding and occupation of sunlit leaves favors defense response and development in the flea beetle, Altica brevicollis coryletorum–a pest of Corylus avellana. PLoS ONE. 2015a; 10(4): e0126072.
- View Article
- Google Scholar
13. Muller O, Hirose T, Werger MJA, Hikosaka K. Optimal use of leaf nitrogen explains seasonal changes in leaf nitrogen content of an understorey evergreen shrub. Annals of Botany. 2011; 108: 529–536. pmid:21757476
- View Article
- PubMed/NCBI
- Google Scholar
14. Migita C, Chiba Y, Tange T. Seasonal and spatial variations in leaf nitrogen content and resorption in a Quercus serrata canopy. Tree Physiology. 2007; 27: 63–70. pmid:17169907
- View Article
- PubMed/NCBI
- Google Scholar
15. Ayabe Y, Minoura T, Hijii N. Plasticity in resource use by the leafminer moth Phyllocnistis sp. in response to variations in host plant resources over space and time. Journal of Forestry Research. 2015; 20:213–221.
- View Article
- Google Scholar
16. Łukowski A., Mąderek E., Giertych Karolewski P. Sex ratio and body mass of adult herbivorous beetles depend on time of occurrence and light conditions. PLoS ONE. 2015; 10(12) e0144718. pmid:26657564
- View Article
- PubMed/NCBI
- Google Scholar
17. Nelson WA, Bjørnstad ON, Yamanaka T. Recurrent insect outbreaks caused by temperature driven changes in system stability. Science. 2013; 341: 796–799. pmid:23907532
- View Article
- PubMed/NCBI
- Google Scholar
18. Diaz R, Aguirre C, Wheeler GS, Lapointe SL, Rosskopf E, Overholt WA. Differential performance of Tropical Soda Apple and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae) in open and shaded habitats. Environmental Entomology. 2011; 40:1437–1447. pmid:22217759
- View Article
- PubMed/NCBI
- Google Scholar
19. Uyi OO, Zachariades C, Hill MP, Conlong D. The nocturnal larvae of a specialist folivore perform better on Chromolaena odorata leaves from a shaded environment. Entomologia Experimentalis et Applicata. 2015; 156: 187–199.
- View Article
- Google Scholar
20. Roberts MR, Paul ND. Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytologist. 2006; 170: 677–699. pmid:16684231
- View Article
- PubMed/NCBI
- Google Scholar
21. Zhang LL, Wen DZ. Structural and physiological responses of two invasive weeds, Mikania micrantha and Chromolaena odorata to contrasting light and soil water conditions. Journal of Plant Research. 2009; 122:69–79. pmid:19030958
- View Article
- PubMed/NCBI
- Google Scholar
22. Bryant JP, Chapin FS III, Klein DR. Carbon: nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos. 1983; 40: 357–368.
- View Article
- Google Scholar
23. Bryant JP, Chapin FS III, Reichardt PB, Clausen TP. Response of winter chemical defence in Alaska paper birch and green alder to manipulation of plant carbon: nutrient balance. Oecologia. 1987; 72: 510–514. pmid:28312511
- View Article
- PubMed/NCBI
- Google Scholar
24. Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Quarterly Review of Biology. 1992; 67: 283–335.
- View Article
- Google Scholar
25. Koricheva J, Larsson S, Haukioja E, Keinänen M. Regulation plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos. 1998; 83: 212–226.
- View Article
- Google Scholar
26. Rowe WJ, Potter DA. Shading effects on susceptibility of Rosa spp. to defoliation by Popillia japonica (Coleoptera: Scarabaeidae). Environmental Entomology. 2000; 29: 502–508.
- View Article
- Google Scholar
27. Moore LV, Myers JH, Eng R. Western tent caterpillars prefer the sunny side of the tree but why? Oikos. 1988; 51: 321–326.
- View Article
- Google Scholar
28. Sipura M, Tahvanainen J. Shading enhances the quality of willow leaves to leaf beetles—but does it matter? Oikos. 2000; 91: 550–558.
- View Article
- Google Scholar
29. Ruusila V, Morin J, van Ooik T, Saloniemi I, Ossipov V, Haukioja E. A short-lived herbivore on a long-lived host: tree resistance to herbivory depends on leaf age. Oikos. 2005; 108: 99–104.
- View Article
- Google Scholar
30. Zachariades C, Day M, Muniappan R, Reddy GVP. Chromolaena odorata (L.) King and Robinson (Asteraceae). In: Muniappan R, Reddy GVP, Raman A, editors. Biological control of tropical weeds using arthropods. Cambridge University Press, UK; 2009. pp. 130–160.
31. Uyi OO, Ekhator F, Ikuenobe CE, Borokini TI, Aigbokhan EI, Egbon IN et al. Chromolaena odorata invasion in Nigeria: A case for coordinated biological control. Management of Biological Invasions. 2014; 5: 377–393.
- View Article
- Google Scholar
32. Paterson ID, Zachariades C. ISSRs indicate that Chromolaena odorata invading southern Africa originates in Jamaica or Cuba. Biological Control. 2013; 66:132–139.
- View Article
- Google Scholar
33. Kluge RL, Caldwell PM. Host specificity of Pareuchaetes insulata (Lep.: Arctiidae), a biological control agent for Chromolaena odorata (Compositae). Entomophaga 1993; 38: 451–457.
- View Article
- Google Scholar
34. Uyi OO, Zachariades C, Hill MP. The life history traits of the arctiine moth Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. African Entomology. 2014b; 22: 611–624.
- View Article
- Google Scholar
35. Dube N, Assefa Y, Zachariades C, Olckers T, Conlong D. Genetic diversity in Pareuchaetes insulata and its implications for biological control of Chromolaena odorata. BioControl. 2014; 59: 253–262
- View Article
- Google Scholar
36. Zachariades C, Uyi OO, Dube N, Strathie LW, Muir D, Conlong DE, Assefa Y. Biological control of Chromolaena odorata: Pareuchaetes insulata spreads its wings. Proceedings of the South African Sugarcane Technologists Association. 2016; 89: 291–306.
- View Article
- Google Scholar
37. Steinbauer MJ. Specific leaf weight as an indicator of juvenile leaf toughness in Tasmanian bluegum (Eucalyptus globulus ssp. globulus): implications for insect defoliation. Australian Forestry. 2001; 64:32–37.
- View Article
- Google Scholar
38. Watanabe FS, Olsen SR. Test of an ascorbic acid method for determining phosphorus in water and NaHCO₃ extracts from soil. Soil Science Society of America Proceedings. 1965; 29: 677–678.
- View Article
- Google Scholar
39. Marais JP. Evaluation of acid hydrolysis procedures for the rapid determination of total non-structural carbohydrates in plant species. Agrochemophysica. 1979; 11: 1–3.
- View Article
- Google Scholar
40. van Soest PJ. Use of detergents in the analysis of fibrous feeds II. A rapid method for the determination of fibre and lignin. Journal of the Association of Official Analytical Chemists. 1963; 46: 829–835.
- View Article
- Google Scholar
41. Uyi OO, Hill MP, Zachariades C. Variation in host plant has no effect on the performance and fitness-related traits of the specialist herbivore, Pareuchaetes insulata. Entomologia Experimentalis et Applicata. 2014; 153: 64–75.
- View Article
- Google Scholar
42. Uyi O, Egbon IN, Igbinosa IB. Discovery of, and studies on Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae) in southern Nigeria. International Journal of Tropical Insect Science. 2011; 31: 199–203.
- View Article
- Google Scholar
43. Maw MG. Biology of the tortoise beetle, Cassida hemisphaerica (Coleoptera: Chrysomelidae), a possible biological control agent for bladder campion, Silene cucubalus (Caryophyllaceae), in Canada. Canadian Entomologist. 1976; 108: 945–954.
- View Article
- Google Scholar
44. Connor EF. Effects of the light environment on oviposition preference and survival of a leaf-mining moth, Cameraria hamadryadella (Lepidoptera: Gracillariidae), on Quercus alba L. Ecological Entomology. 2006; 31: 179–184.
- View Article
- Google Scholar
45. Weih M, Karlsson PS. Growth response of mountain birch to air and soil temperature: is increasing leaf-nitrogen content an acclimation to lower air temperature? New Phytologist. 2001; 150: 147–155.
- View Article
- Google Scholar
46. Muller O, Hikosaka K, Hirose T. Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub. Oecologia. 2005; 143: 501–508. pmid:15761779
- View Article
- PubMed/NCBI
- Google Scholar
47. Muth NZ, Kluger EC, Levy JH, Edwards MJ, Niesenbaum RA. Increased per capita herbivory in the shade: necessity, feedback, or luxury consumption? Ecoscience. 2008; 15: 182–188.
- View Article
- Google Scholar
48. Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ et al. Global patterns of leaf mechanical properties. Ecology Letters. 2011; 14: 301–312. pmid:21265976
- View Article
- PubMed/NCBI
- Google Scholar
49. Uesugi A. The slow-growth high-mortality hypothesis: direct experimental support in a leafmining fly. Ecological Entomology. 2015; 40: 221–228
- View Article
- Google Scholar
50. Kariyat RR, Portman SL. Plant–herbivore interactions: Thinking beyond larval. American Journal of Botany. 2012; 103:1–3.
- View Article
- Google Scholar
51. Honěk A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos. 1993; 66: 483–492.
- View Article
- Google Scholar
52. Fordyce JA, Shapiro AM. Another perspective on the slow-growth/high-mortality hypothesis: chilling effects on swallowtail larvae. Ecology. 2003; 84: 263–268.
- View Article
- Google Scholar
53. Huberty AF, Denno RF. Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia. 2006; 149: 444–455. pmid:16794833
- View Article
- PubMed/NCBI
- Google Scholar
54. Raubenheimer AD, Lee KP, Simpson SJ. Does Bertrand’s rule apply to macronutrients? Proceedings of the Royal Society, London [Biol]. 2005; 272: 2429–2434.
- View Article
- Google Scholar
55. Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93: 1002–1015. pmid:22764487
- View Article
- PubMed/NCBI
- Google Scholar
56. Uyi OO, Zachariades C, Hill MP, McConnachie AJ. Temperature-dependent performance and potential distribution of Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. BioControl. 2016b; 61: 815–825.
- View Article
- Google Scholar
57. Uyi OO, Zachariades C, Marais E, Hill MP. Reduced mobility but high survival: thermal tolerance and locomotor response of the specialist herbivore, Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae), to low temperatures. Bulletin of Entomological Research. 2017; 107: 448–457. pmid:27974070
- View Article
- PubMed/NCBI
- Google Scholar
58. Conner WE. Utethesia ornatrix, the ornate Arctiid tiger moths and woolly bears: Behavior, Ecology, and Evolution of the Arctiidae. Oxford University Press; 2009.
59. Macel M. Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochemistry Review. 2011; 10: 75–82.
- View Article
- Google Scholar
60. Cornell HV, Hawkins BA. Survival patterns and mortality sources of herbivorous insects: some demographic trends. American Naturalist. 1995; 145: 563–593.
- View Article
- Google Scholar
61. Bezzerides A, Yong T, Bezzerides J, Husseini J, Ladau J, Eisner M et al. Plant-derived pyrrolizidine alkaloid protects eggs of a moth (Utetheisa ornatrix) against a parasitoid wasp (Trichogramma ostriniae). Proceedings of the National Academy of Science USA. 2004; 101: 9029–9032.
- View Article
- Google Scholar
62. LaMunyon CW, Eisner T. Postcopulatory sexual selection in an arctiid moth (Utetheisa ornatrix). Proceedings of the National Academy of Science USA. 1993; 90:4689–4692.
- View Article
- Google Scholar
63. McFadyen RE. Parasitoids of the arctiid moth Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae), an introduced biocontrol agent against the weed Chromolaena odorata (Asteraceae), in Asia and Africa. Entomophaga. 1997; 42: 467–470.
- View Article
- Google Scholar

[ref1] 1. Myers JH, Post BJ. Plant nitrogen and fluctuations of insect populations: a test with the cinnabar moth-tansy ragwort system. Oecologia. 1981; 48: 151–156. pmid:28309793
View Article
PubMed/NCBI
Google Scholar

[2] View Article

[3] PubMed/NCBI

[4] Google Scholar

[ref2] 2. Awmack CS, Leather SR. Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology. 2002; 47: 817–844. pmid:11729092
View Article
PubMed/NCBI
Google Scholar

[6] View Article

[7] PubMed/NCBI

[8] Google Scholar

[ref3] 3. Uyi OO, Zachariades C, Hill MP. Nitrogen fertilization improves growth of Chromolaena odorata (Asteraceae) and the performance of the biological control agent, Pareuchaetes insulata (Erebidae). Biocontrol Science and Technology. 2016; 26: 373–385.
View Article
Google Scholar

[10] View Article

[11] Google Scholar

[ref4] 4. Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R. Variability in plant nutrients reduces insect herbivore performance growth and mortality. Nature. 2016; 539(7629): 425–427. pmid:27749815
View Article
PubMed/NCBI
Google Scholar

[13] View Article

[14] PubMed/NCBI

[15] Google Scholar

[ref5] 5. Osier TL, Jennings SM. Variability in host plant quality for the larvae of a polyphagous insect folivore in midseason: the impact of light on three deciduous sapling species. Entomologia Experimentalis et Applicata. 2007; 123: 159–166.
View Article
Google Scholar

[17] View Article

[18] Google Scholar

[ref6] 6. Karolewski P, Giertych MJ, Żmuda M, Jagodziński AM, Oleksyn J. Season and light affect constitutive defenses of understory shrub species against folivorous insects. Acta Oecologica. 2013; 53: 19–32.
View Article
Google Scholar

[20] View Article

[21] Google Scholar

[ref7] 7. Carvalho S, Macel M, Mulder PPJ, Skidmore A, van der Putten WH. Chemical variation in Jacobaea vulgaris is influenced by the interaction of season and vegetation successional stage. Phytochemistry. 2014; 99: 86–94. pmid:24412324
View Article
PubMed/NCBI
Google Scholar

[23] View Article

[24] PubMed/NCBI

[25] Google Scholar

[ref8] 8. Uyi OO, Uwagiahanor BI, Ejomah AJ. The nocturnal larvae of a specialist folivore prefer Chromolaena odorata (L.) foliage from a sunny environment, but does it matter? Arthropod-Plant Interactions. 2017; 11: 603–611.
View Article
Google Scholar

[27] View Article

[28] Google Scholar

[ref9] 9. Alonso C, Herrera CM. Seasonal variation in leaf characteristics and food selection by larval noctuids on an evergreen Mediterranean shrub. Acta Oecologica. 2000; 21: 257–265.
View Article
Google Scholar

[30] View Article

[31] Google Scholar

[ref10] 10. Gripenberg S, Salminen J, Roslin T A tree in the eyes of a moth—temporal variation in oak leaf quality and leaf-miner performance. Oikos. 2007; 116: 592–600.
View Article
Google Scholar

[33] View Article

[34] Google Scholar

[ref11] 11. Sarfraz RM, Kharouba HM, Myers JH. Tent caterpillars are robust to variation in leaf phenology and quality in two thermal environments. Bulletin of Entomological Research. 2013; 103: 522–529. pmid:23464617
View Article
PubMed/NCBI
Google Scholar

[36] View Article

[37] PubMed/NCBI

[38] Google Scholar

[ref12] 12. Łukowski A, Giertych MJ, Zadworny M, Mucha J, Karolewski P. Preferential feeding and occupation of sunlit leaves favors defense response and development in the flea beetle, Altica brevicollis coryletorum–a pest of Corylus avellana. PLoS ONE. 2015a; 10(4): e0126072.
View Article
Google Scholar

[40] View Article

[41] Google Scholar

[ref13] 13. Muller O, Hirose T, Werger MJA, Hikosaka K. Optimal use of leaf nitrogen explains seasonal changes in leaf nitrogen content of an understorey evergreen shrub. Annals of Botany. 2011; 108: 529–536. pmid:21757476
View Article
PubMed/NCBI
Google Scholar

[43] View Article

[44] PubMed/NCBI

[45] Google Scholar

[ref14] 14. Migita C, Chiba Y, Tange T. Seasonal and spatial variations in leaf nitrogen content and resorption in a Quercus serrata canopy. Tree Physiology. 2007; 27: 63–70. pmid:17169907
View Article
PubMed/NCBI
Google Scholar

[47] View Article

[48] PubMed/NCBI

[49] Google Scholar

[ref15] 15. Ayabe Y, Minoura T, Hijii N. Plasticity in resource use by the leafminer moth Phyllocnistis sp. in response to variations in host plant resources over space and time. Journal of Forestry Research. 2015; 20:213–221.
View Article
Google Scholar

[51] View Article

[52] Google Scholar

[ref16] 16. Łukowski A., Mąderek E., Giertych Karolewski P. Sex ratio and body mass of adult herbivorous beetles depend on time of occurrence and light conditions. PLoS ONE. 2015; 10(12) e0144718. pmid:26657564
View Article
PubMed/NCBI
Google Scholar

[54] View Article

[55] PubMed/NCBI

[56] Google Scholar

[ref17] 17. Nelson WA, Bjørnstad ON, Yamanaka T. Recurrent insect outbreaks caused by temperature driven changes in system stability. Science. 2013; 341: 796–799. pmid:23907532
View Article
PubMed/NCBI
Google Scholar

[58] View Article

[59] PubMed/NCBI

[60] Google Scholar

[ref18] 18. Diaz R, Aguirre C, Wheeler GS, Lapointe SL, Rosskopf E, Overholt WA. Differential performance of Tropical Soda Apple and its biological control agent Gratiana boliviana (Coleoptera: Chrysomelidae) in open and shaded habitats. Environmental Entomology. 2011; 40:1437–1447. pmid:22217759
View Article
PubMed/NCBI
Google Scholar

[62] View Article

[63] PubMed/NCBI

[64] Google Scholar

[ref19] 19. Uyi OO, Zachariades C, Hill MP, Conlong D. The nocturnal larvae of a specialist folivore perform better on Chromolaena odorata leaves from a shaded environment. Entomologia Experimentalis et Applicata. 2015; 156: 187–199.
View Article
Google Scholar

[66] View Article

[67] Google Scholar

[ref20] 20. Roberts MR, Paul ND. Seduced by the dark side: integrating molecular and ecological perspectives on the influence of light on plant defence against pests and pathogens. New Phytologist. 2006; 170: 677–699. pmid:16684231
View Article
PubMed/NCBI
Google Scholar

[69] View Article

[70] PubMed/NCBI

[71] Google Scholar

[ref21] 21. Zhang LL, Wen DZ. Structural and physiological responses of two invasive weeds, Mikania micrantha and Chromolaena odorata to contrasting light and soil water conditions. Journal of Plant Research. 2009; 122:69–79. pmid:19030958
View Article
PubMed/NCBI
Google Scholar

[73] View Article

[74] PubMed/NCBI

[75] Google Scholar

[ref22] 22. Bryant JP, Chapin FS III, Klein DR. Carbon: nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos. 1983; 40: 357–368.
View Article
Google Scholar

[77] View Article

[78] Google Scholar

[ref23] 23. Bryant JP, Chapin FS III, Reichardt PB, Clausen TP. Response of winter chemical defence in Alaska paper birch and green alder to manipulation of plant carbon: nutrient balance. Oecologia. 1987; 72: 510–514. pmid:28312511
View Article
PubMed/NCBI
Google Scholar

[80] View Article

[81] PubMed/NCBI

[82] Google Scholar

[ref24] 24. Herms DA, Mattson WJ. The dilemma of plants: to grow or defend. Quarterly Review of Biology. 1992; 67: 283–335.
View Article
Google Scholar

[84] View Article

[85] Google Scholar

[ref25] 25. Koricheva J, Larsson S, Haukioja E, Keinänen M. Regulation plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos. 1998; 83: 212–226.
View Article
Google Scholar

[87] View Article

[88] Google Scholar

[ref26] 26. Rowe WJ, Potter DA. Shading effects on susceptibility of Rosa spp. to defoliation by Popillia japonica (Coleoptera: Scarabaeidae). Environmental Entomology. 2000; 29: 502–508.
View Article
Google Scholar

[90] View Article

[91] Google Scholar

[ref27] 27. Moore LV, Myers JH, Eng R. Western tent caterpillars prefer the sunny side of the tree but why? Oikos. 1988; 51: 321–326.
View Article
Google Scholar

[93] View Article

[94] Google Scholar

[ref28] 28. Sipura M, Tahvanainen J. Shading enhances the quality of willow leaves to leaf beetles—but does it matter? Oikos. 2000; 91: 550–558.
View Article
Google Scholar

[96] View Article

[97] Google Scholar

[ref29] 29. Ruusila V, Morin J, van Ooik T, Saloniemi I, Ossipov V, Haukioja E. A short-lived herbivore on a long-lived host: tree resistance to herbivory depends on leaf age. Oikos. 2005; 108: 99–104.
View Article
Google Scholar

[99] View Article

[100] Google Scholar

[ref30] 30. Zachariades C, Day M, Muniappan R, Reddy GVP. Chromolaena odorata (L.) King and Robinson (Asteraceae). In: Muniappan R, Reddy GVP, Raman A, editors. Biological control of tropical weeds using arthropods. Cambridge University Press, UK; 2009. pp. 130–160.

[ref31] 31. Uyi OO, Ekhator F, Ikuenobe CE, Borokini TI, Aigbokhan EI, Egbon IN et al. Chromolaena odorata invasion in Nigeria: A case for coordinated biological control. Management of Biological Invasions. 2014; 5: 377–393.
View Article
Google Scholar

[103] View Article

[104] Google Scholar

[ref32] 32. Paterson ID, Zachariades C. ISSRs indicate that Chromolaena odorata invading southern Africa originates in Jamaica or Cuba. Biological Control. 2013; 66:132–139.
View Article
Google Scholar

[106] View Article

[107] Google Scholar

[ref33] 33. Kluge RL, Caldwell PM. Host specificity of Pareuchaetes insulata (Lep.: Arctiidae), a biological control agent for Chromolaena odorata (Compositae). Entomophaga 1993; 38: 451–457.
View Article
Google Scholar

[109] View Article

[110] Google Scholar

[ref34] 34. Uyi OO, Zachariades C, Hill MP. The life history traits of the arctiine moth Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. African Entomology. 2014b; 22: 611–624.
View Article
Google Scholar

[112] View Article

[113] Google Scholar

[ref35] 35. Dube N, Assefa Y, Zachariades C, Olckers T, Conlong D. Genetic diversity in Pareuchaetes insulata and its implications for biological control of Chromolaena odorata. BioControl. 2014; 59: 253–262
View Article
Google Scholar

[115] View Article

[116] Google Scholar

[ref36] 36. Zachariades C, Uyi OO, Dube N, Strathie LW, Muir D, Conlong DE, Assefa Y. Biological control of Chromolaena odorata: Pareuchaetes insulata spreads its wings. Proceedings of the South African Sugarcane Technologists Association. 2016; 89: 291–306.
View Article
Google Scholar

[118] View Article

[119] Google Scholar

[ref37] 37. Steinbauer MJ. Specific leaf weight as an indicator of juvenile leaf toughness in Tasmanian bluegum (Eucalyptus globulus ssp. globulus): implications for insect defoliation. Australian Forestry. 2001; 64:32–37.
View Article
Google Scholar

[121] View Article

[122] Google Scholar

[ref38] 38. Watanabe FS, Olsen SR. Test of an ascorbic acid method for determining phosphorus in water and NaHCO₃ extracts from soil. Soil Science Society of America Proceedings. 1965; 29: 677–678.
View Article
Google Scholar

[124] View Article

[125] Google Scholar

[ref39] 39. Marais JP. Evaluation of acid hydrolysis procedures for the rapid determination of total non-structural carbohydrates in plant species. Agrochemophysica. 1979; 11: 1–3.
View Article
Google Scholar

[127] View Article

[128] Google Scholar

[ref40] 40. van Soest PJ. Use of detergents in the analysis of fibrous feeds II. A rapid method for the determination of fibre and lignin. Journal of the Association of Official Analytical Chemists. 1963; 46: 829–835.
View Article
Google Scholar

[130] View Article

[131] Google Scholar

[ref41] 41. Uyi OO, Hill MP, Zachariades C. Variation in host plant has no effect on the performance and fitness-related traits of the specialist herbivore, Pareuchaetes insulata. Entomologia Experimentalis et Applicata. 2014; 153: 64–75.
View Article
Google Scholar

[133] View Article

[134] Google Scholar

[ref42] 42. Uyi O, Egbon IN, Igbinosa IB. Discovery of, and studies on Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae) in southern Nigeria. International Journal of Tropical Insect Science. 2011; 31: 199–203.
View Article
Google Scholar

[136] View Article

[137] Google Scholar

[ref43] 43. Maw MG. Biology of the tortoise beetle, Cassida hemisphaerica (Coleoptera: Chrysomelidae), a possible biological control agent for bladder campion, Silene cucubalus (Caryophyllaceae), in Canada. Canadian Entomologist. 1976; 108: 945–954.
View Article
Google Scholar

[139] View Article

[140] Google Scholar

[ref44] 44. Connor EF. Effects of the light environment on oviposition preference and survival of a leaf-mining moth, Cameraria hamadryadella (Lepidoptera: Gracillariidae), on Quercus alba L. Ecological Entomology. 2006; 31: 179–184.
View Article
Google Scholar

[142] View Article

[143] Google Scholar

[ref45] 45. Weih M, Karlsson PS. Growth response of mountain birch to air and soil temperature: is increasing leaf-nitrogen content an acclimation to lower air temperature? New Phytologist. 2001; 150: 147–155.
View Article
Google Scholar

[145] View Article

[146] Google Scholar

[ref46] 46. Muller O, Hikosaka K, Hirose T. Seasonal changes in light and temperature affect the balance between light harvesting and light utilisation components of photosynthesis in an evergreen understory shrub. Oecologia. 2005; 143: 501–508. pmid:15761779
View Article
PubMed/NCBI
Google Scholar

[148] View Article

[149] PubMed/NCBI

[150] Google Scholar

[ref47] 47. Muth NZ, Kluger EC, Levy JH, Edwards MJ, Niesenbaum RA. Increased per capita herbivory in the shade: necessity, feedback, or luxury consumption? Ecoscience. 2008; 15: 182–188.
View Article
Google Scholar

[152] View Article

[153] Google Scholar

[ref48] 48. Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ et al. Global patterns of leaf mechanical properties. Ecology Letters. 2011; 14: 301–312. pmid:21265976
View Article
PubMed/NCBI
Google Scholar

[155] View Article

[156] PubMed/NCBI

[157] Google Scholar

[ref49] 49. Uesugi A. The slow-growth high-mortality hypothesis: direct experimental support in a leafmining fly. Ecological Entomology. 2015; 40: 221–228
View Article
Google Scholar

[159] View Article

[160] Google Scholar

[ref50] 50. Kariyat RR, Portman SL. Plant–herbivore interactions: Thinking beyond larval. American Journal of Botany. 2012; 103:1–3.
View Article
Google Scholar

[162] View Article

[163] Google Scholar

[ref51] 51. Honěk A. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos. 1993; 66: 483–492.
View Article
Google Scholar

[165] View Article

[166] Google Scholar

[ref52] 52. Fordyce JA, Shapiro AM. Another perspective on the slow-growth/high-mortality hypothesis: chilling effects on swallowtail larvae. Ecology. 2003; 84: 263–268.
View Article
Google Scholar

[168] View Article

[169] Google Scholar

[ref53] 53. Huberty AF, Denno RF. Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia. 2006; 149: 444–455. pmid:16794833
View Article
PubMed/NCBI
Google Scholar

[171] View Article

[172] PubMed/NCBI

[173] Google Scholar

[ref54] 54. Raubenheimer AD, Lee KP, Simpson SJ. Does Bertrand’s rule apply to macronutrients? Proceedings of the Royal Society, London [Biol]. 2005; 272: 2429–2434.
View Article
Google Scholar

[175] View Article

[176] Google Scholar

[ref55] 55. Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93: 1002–1015. pmid:22764487
View Article
PubMed/NCBI
Google Scholar

[178] View Article

[179] PubMed/NCBI

[180] Google Scholar

[ref56] 56. Uyi OO, Zachariades C, Hill MP, McConnachie AJ. Temperature-dependent performance and potential distribution of Pareuchaetes insulata, a biological control agent of Chromolaena odorata in South Africa. BioControl. 2016b; 61: 815–825.
View Article
Google Scholar

[182] View Article

[183] Google Scholar

[ref57] 57. Uyi OO, Zachariades C, Marais E, Hill MP. Reduced mobility but high survival: thermal tolerance and locomotor response of the specialist herbivore, Pareuchaetes insulata (Walker) (Lepidoptera: Erebidae), to low temperatures. Bulletin of Entomological Research. 2017; 107: 448–457. pmid:27974070
View Article
PubMed/NCBI
Google Scholar

[185] View Article

[186] PubMed/NCBI

[187] Google Scholar

[ref58] 58. Conner WE. Utethesia ornatrix, the ornate Arctiid tiger moths and woolly bears: Behavior, Ecology, and Evolution of the Arctiidae. Oxford University Press; 2009.

[ref59] 59. Macel M. Attract and deter: a dual role for pyrrolizidine alkaloids in plant-insect interactions. Phytochemistry Review. 2011; 10: 75–82.
View Article
Google Scholar

[190] View Article

[191] Google Scholar

[ref60] 60. Cornell HV, Hawkins BA. Survival patterns and mortality sources of herbivorous insects: some demographic trends. American Naturalist. 1995; 145: 563–593.
View Article
Google Scholar

[193] View Article

[194] Google Scholar

[ref61] 61. Bezzerides A, Yong T, Bezzerides J, Husseini J, Ladau J, Eisner M et al. Plant-derived pyrrolizidine alkaloid protects eggs of a moth (Utetheisa ornatrix) against a parasitoid wasp (Trichogramma ostriniae). Proceedings of the National Academy of Science USA. 2004; 101: 9029–9032.
View Article
Google Scholar

[196] View Article

[197] Google Scholar

[ref62] 62. LaMunyon CW, Eisner T. Postcopulatory sexual selection in an arctiid moth (Utetheisa ornatrix). Proceedings of the National Academy of Science USA. 1993; 90:4689–4692.
View Article
Google Scholar

[199] View Article

[200] Google Scholar

[ref63] 63. McFadyen RE. Parasitoids of the arctiid moth Pareuchaetes pseudoinsulata (Lepidoptera: Arctiidae), an introduced biocontrol agent against the weed Chromolaena odorata (Asteraceae), in Asia and Africa. Entomophaga. 1997; 42: 467–470.
View Article
Google Scholar

[202] View Article

[203] Google Scholar

Figures

Abstract

Introduction

Materials and methods

Study organisms

Measurement of physical and chemical characteristics of leaves

Development and reproductive performance of Pareuchaetes insulata

Larval preference test

Statistical analysis

Results

Leaf characteristics

Developmental and reproductive performance of Pareuchaetes insulata

Larval preference

Discussion

Acknowledgments

References