Biological Control 106 (2017) 83–88
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Biological Control 106 (2017) 83–88 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Interaction between temperature and water nutrient levels on the fitness of Eccritotarsus catarinensis (Hemiptera: Miridae), a biological control agent of water hyacinth ⇑ Mohannad Ismail a, , Stephen G. Compton a, Margot Brooks b a Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa b Department of Biochemistry and Microbiology, Rhodes University, Grahamstown, South Africa highlights graphical abstract Three temperature for each nutrient level: Fitness traits of insect herbivores may High Medium Low 20°°C, 25 C and 30 ° C 140 a b b 120 c change with environmental c 100 High N 80 d 60 de d conditions. e 40 20 fecundity(numbereggs) Lifetime of 0 We tested the interaction of 20°C 25°C 30°C Medium N 140 a b 120 c temperature and nutrient status of d Eccritotarsus catarinensis 100 d 80 Low N 60 e water on the fitness of E. catarinensis. f f 40 20 g adults) of (number Realised fecundity The reduction in fitness due to higher 0 Eichhornia crassipes 20°C 25°C 30°C temperatures was significantly enhanced when combined with low nutritional status. The insect followed non-linear and linear responses, depending on temperatures and water nutrient status. article info abstract Article history: Fitness traits of insect herbivores of aquatic weeds may change with environmental conditions including Received 24 June 2016 temperature and water nutrient levels. Both of these factors are likely to increase due to changes in global Revised 7 December 2016 weather patterns and human activity. We tested the interaction of temperature and nutrient status on Accepted 4 January 2017 the fitness of Eccritotarsus catarinensis, a biocontrol agent against the invasive aquatic weed, water hya- Available online 5 January 2017 cinth Eichhornia crassipes. Several life history traits were evaluated on plants grown at three constant temperatures (20, 25 and 30 °C) combined with three nutrient levels: oligotrophic (low), mesotrophic Keywords: (medium), and eutrophic (high). When the two factors are separated, all fitness traits decreased with Fitness traits increasing temperature and decreasing water nutrient levels. The combination of high temperature Herbivore insect Interaction and low water nutrient status had a greater and significant negative effect on some fitness traits: lifetime Invasive aquatic weeds fecundity, realized fecundity and nymphal survival. The relationship between insect fitness traits and water nutrient status followed different patterns depending on temperature: a monotonic, but non- linear response at 20 °C, where fitness was highest at medium water nutrient status and reduced at low and high water nutrient status; and a linear monotonic response at 25 °C, where fitness increased with increasing water nutrient status. At 30 °C fitness traits were equal on plants grown in water with high and medium nutrient status and lower on those grown in water with low nutrient status. We demonstrated that a combination of low nutrient waters with higher temperatures would hamper the efficacy of this agent. Our results suggested that the negative impact of the herbivorous insects on the aquatic weed would be most successful on vigorous plants, applicable for both mesotrophic and eutrophic nutrient levels, particularly in temperate areas. Ó 2017 Elsevier Inc. All rights reserved. ⇑ Corresponding author. Address: Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan Botanical Garden/Institute, Chinese Academy of Sciences, Wuhan, China. E-mail address: [email protected] (M. Ismail). http://dx.doi.org/10.1016/j.biocontrol.2017.01.001 1049-9644/Ó 2017 Elsevier Inc. All rights reserved. 84 M. Ismail et al. / Biological Control 106 (2017) 83–88 1. Introduction influence of temperature was not considered in any of these stud- ies. We believe that the impact of this kind of interaction remains The invasive aquatic weed, Eichhornia crassipes Mart (Solms- relatively poorly understood and in need of investigation. Laubach) (Pontederiaceae), commonly known as water hyacinth, A sap-sucking bug, Eccritotarsus catarinensis Carvalho (Hemi- has been widely distributed from its origin in South America ptera: Miridae), which has been released in South Africa for the throughout tropical, subtropical and some warmer temperate control of E. crassipes, provides an opportunity to study the impact regions of the world where it is extremely invasive and problem- of interactions on the fitness of the insects. Adults and nymphs atic in freshwater ecosystems (Julien et al., 1996; Hill, 2003). Its feed gregariously on the leaves of E. crassipes, resulting in chlorosis abundance is linked to temperature (Hoveka et al., 2016; Shu and leaf loss (Hill et al., 1999). Nymphal development time is sig- et al., 2014) and the availability of resources in the water, particu- nificantly shorter on young leaves, which typically have a higher larly nitrogen (N) (Gossett and Norris, 1971; Gopal, 1987). The nutrient content than old leaves (Burke et al., 2014). There are most promising method for reducing populations of E. crassipes is two geographically separated strains of E. catarinensis, originating through the release of host specific biological control agents (e.g. from Brazil and Peru respectively. In this study we used the Peru- DeLoach et al., 1980; Julien, 1987; Hill and Cilliers, 1999; Coetzee vian strain, since it develops better at 30 °C than the Brazilian et al., 2011; Tipping et al., 2011). However, despite the successful strain (Ismail and Brooks, 2016). establishment of biological control agents against E. crassipes in We investigated whether the fitness traits of E. catarinensis many areas (e.g. Jayanth, 1988; Hill and Cilliers, 1999; Julien and would change in response to nutrient levels in the water according Orapa, 2000; Williams et al., 2007), they have been less successful to the plant stress, the plant vigour or the N limitation hypotheses. in others (Julien, 1987; Hill and Olckers, 2001; Coetzee and Hill, Based on a prediction that fitness traits would decrease linearly 2008). This has been ascribed to several factors including the local with increasing temperature, we tested whether or not the interac- climate and water nutrient status (Hill and Olckers, 2001; Byrne tion between temperature and water nutrient levels would influ- et al., 2003; Moran, 2006; Center et al., 2014). ence the types of insect performance responses, and whether While temperature may be a major factor in determining the these would be linear or non-linear. fitness of insect herbivores (Bauerfeind and Fischer, 2014; Ismail and Brooks, 2016), fitness can also be influenced by the nutritional 2. Material and methods quality of the host plants on which the insects feed (Crawley, 1989; Awmack and Leather, 2002; Throop and Lerdau, 2004; Sisodia and 2.1. Rearing of Eichhornia crassipes Singh, 2012). The nutritional quality of plants is particularly dependent on the levels of nitrogen in the environment in which Eichhornia crassipes plants were obtained in August 2013 from they grow (Hogendorp et al., 2006; Larbat et al., 2016). Human stock cultures maintained at a high level of nitrogen and exposed actions such as the misuse of artificial fertilisers and poor treat- to ambient day length and temperature. The plants were grown ment of sewage often lead to unnaturally elevated levels of avail- in 40 cm  60 cm plastic tubs filled with 50L of tap water with able N in the environment (Galloway et al., 2003). Any increase three nutrient levels (6 tubs for each nutrient level): oligotrophic in N availability could affect the fitness of herbivore insects À (low, only tap water), mesotrophic (medium: 1.5 mg l 1), and (Bownes et al., 2013a; Sarfraz et al., 2009), due to the consequent À eutrophic (high: 6.25 mg l 1) based on nitrogen concentrations effect on the nutrient content of the host plants. (Reddy et al., 1989), using a commercial water soluble fertilizer Early hypotheses proposed to explain the responses of insect (Multifeed Classic Fertilizer, 19N: 8P: 16K) in combination with a herbivores to the amount of N available in plant tissues include À commercial iron chelate (33 mg l 1) to prevent chlorosis (Coetzee the Plant Stress hypothesis originally proposed by White (1984), et al., 2007). The selected concentrations are the averages of nitro- the Plant Vigour hypothesis of Price (1991) and the ‘‘Nitrogen lim- gen levels reflected in the range present in South African water itation hypothesis” put forward by White et al. (1993). However, bodies (Coetzee and Hill, 2012). Water in the tubs with high and despite the variation in these hypotheses with regard to plant medium nutrient levels was replaced every two weeks. Under quality, they postulated an increase in N available in the plants. these nutrient conditions, it has been shown that plant growth De Bruyn et al. (2002) and EnglishLoeb et al. (1997) predicted increases linearly with nutrient uptake (Reddy et al., 1989; the impact of plant quality on the performance of herbivores by Coetzee and Hill, 2012) and it is assumed that nitrogen content the following two responses: a monotonic, linear response, where of the E. crassipes plants increases positively with higher nutrient insect performance increases with increasing plant quality; and a levels (Burke et al., 2014). Plants grown under high nutrient levels quadratic (non-monotonic or non-linear) response, where insect had large green leaves of good quality. Plants that were grown performance is highest on plants of medium quality and reduced under medium nutrient levels had smaller leaves just starting to on plants of low and high quality. yellow. Oligotrophic conditions produced plants with small, yellow Recent research has found indirect effects of temperature on leaves. herbivorous insects through temperature-induced changes in the quality of plant nutrient content (Bauerfeind and Fischer, 2013a, b). However, these investigations did not take into consideration 2.2. Rearing of Eccritotarsus catarinensis the direct effect of the nutritional status of the environment, such as the soil or water in which the plants were grown.