Biological Control 106 (2017) 83–88

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Biological Control

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Interaction between temperature and water nutrient levels on the fitness of Eccritotarsus catarinensis (: ), 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 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 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. Only two pre- In August 2013 around 200 nymphs and adults of the Peruvian vious studies have investigated the combination between temper- strain of E. catarinensis were taken from a stock population and ° ature and nutrient status of the environment: the first involving placed on E. crassipes plants in a 25 C growth chamber to start a the abundance of insects (Lu et al., 2013), and the second the new colony which was maintained in net cages containing  growth and development of plants (Skálová et al., 2015). However, 40 cm 60 cm plastic tubs filled with 50L of eutrophic water. Host no interaction was reported between the two factors in either plants were replaced regularly. study. The effects of high water nutrient conditions on the biolog- ical control of E. crassipes have been investigated, both in respect of 2.3. Experimental design the growth of the weed (Heard and Winterton, 2000; Canavan et al., 2014), and the fitness traits of the biocontrol agents Life history traits of E. catarinensis were compared at three dif- (Coetzee et al., 2007; Bownes et al., 2013b). However, the possible ferent temperatures (20°,25° and 30 °C) while being fed only on M. Ismail et al. / Biological Control 106 (2017) 83–88 85 daughter plants produced from mother plants grown at Table 1 one of each of the three nutrient levels, for each temperature. The mean ± (SE) of fitness traits of E. catarinensis at three constant temperatures. Different letters represent significant differences in all fitness traits among the three The upper temperature limit was set at 30 °C because at temperatures (p < 0.05). temperatures above 30 °C, individuals survive and lay eggs, but these eggs do not develop (personal observation). Numbers of Temperature replicates for the nine treatments (nutrients * temperature) were 20 °C25°C30°C as follows: High (H20 = 10, H25 = 13 and H30 = 15 replicates), Lifetime fecundity 108.45 ± 5.94 a 84.74 ± 7.17 b 45.67 ± 3.61 c Medium (M20 = 10, M25 = 11 and M30 = 14 replicates) and Low Egg hatching% 97.33 ± 0.53 a 92.35 ± 1.58 a 69.73 ± 4.27 b (L20 = 10, L25 = 10 and L30 = 10 replicates). The unequal number Realized fecundity 104.65 ± 6.00 a 77.50 ± 6.66 b 27.10 ± 3.00 c of replicates relates to the necessary exclusion of replicates in Nymphal survival% 98.82 ± 0.39 a 98.71 ± 0.36 a 75.76 ± 5.24 b Sex ratio 0.54 ± 0.01 a 0.53 ± 0.01 a 0.53 ± 0.03 a which the plants had died prematurely during the course of the Male longevity 75.06 ± 2.88 a 49.97 ± 2.06 b 31.76 ± 0.96 c experiment. Female longevity 64.00 ± 3.80 a 45.79 ± 2.30 b 27.82 ± 0.85 c Pairs of E. catarinensis comprising a one-day-old female and a one day old male were placed in individual small plastic Petri dishes (20 mm diameter), each containing moist filter paper and Table 2 one small, fresh E. crassipes leaf taken from plants grown at one The mean ± (SE) of fitness traits of E. catarinensis on water hyacinth at three nutrient of the three water nutrient levels. The dishes were maintained at levels. Different letters represent significant differences in all fitness traits among the nutrient levels (p < 0.05). 25 °C for two days, to allow the E. catarinensis to become reproduc- tively mature. Individual pairs were then transferred to 1L trans- Nutrient level parent plastic bottles, each containing a young E. crassipes plant Eutrophic Mesotrophic Oligotrophic with 5 leaves, grown at the corresponding water nutrient level. Lifetime fecundity 87.46 ± 6.10 a 83.83 ± 7.94 a 55.97 ± 5.95 b The plastic bottles were kept in incubators (Binder GmbH, KBW Egg hatching% 85.97 ± 6.47 a 88.61 ± 3.39 a 80.74 ± 4.75 a 240 (E5.1), Tuttlingen, Germany) with a thermal precision of Realized fecundity 75.15 ± 6.73 a 76.09 ± 8.38 a 44.73 ± 6.32 b ±1 °C, under a photoperiod of 14L: 10D, and humidity 75 ± 10%. Nymphal survival% 91.85 ± 2.10 a 92.83 ± 4.12 a 86.03 ± 5.96 b Each replicate was provided weekly with a new young plant from Sex ratio 0.54 ± 0.01 a 0.51 ± 0.02 a 0.54 ± 0.03 a Male longevity 52.54 ± 3.56 a 48.97 ± 3.56 a 49.93 ± 3.74 a the corresponding water nutrient level, until the death of the Female longevity 48.49 ± 3.85 a 42.14 ± 3.15 b 42.00 ± 3.10 b female insect. Males that died before their female partners did were replaced. The following fitness parameters were measured under the nine 3.1. Lifetime fecundity experimental conditions: Lifetime (total) fecundity: measured by counting offspring emergence holes on the leaves and unhatched The numbers of eggs laid by E. catarinensis females varied eggs. Egg hatching: the proportion of hatched eggs (nymph holes) between treatments, ranging from 40 to 130 (Fig. 1). Fecundity divided by the lifetime fecundity and expressed as a percentage. decreased significantly with increasing temperature Nymphal survival: realised fecundity divided by the number of 2 (v Á2 = 408.27; P < 0.001), with the highest mean numbers of eggs hatched individuals, and expressed as a percentage. Realised produced at 20 °C(Table 1). There was also a positive and signifi- fecundity: number of offspring that reached adulthood. Adult off- cant impact of increased water nutrient level on the number of spring sex ratio: number of females divided by number of adults. 2 eggs laid (v Á2 = 73.33; P < 0.001), with a greater number of eggs Adult longevity: mortality of each couple was monitored daily in eutrophic and mesotrophic nutrient conditions compared to that from the first day of the experiment. in oligotrophic nutrient conditions (Table 2). The interaction between temperature and water nutrient level was also significant 2 (v Á4 = 113.10; P < 0.001) with the highest number of eggs at 20 °C 2.4. Statistical analyses being recorded from plants grown at medium nutrient level, whereas at 25 °C most eggs were laid on plants grown under high Statistical analyses were done using the statistical software R nutrient conditions. Lowest fecundity was recorded at the highest version 2.15.2 (2012-10-26) (R Core Team, 2013). All the tests were temperatures on plants grown under low nutrient conditions carried out with temperature and nutrient level as the main fac- (Fig. 1). The rate of reduction due to temperature change was tors. Egg hatching, nymphal survival and sex ratio were analysed clearly higher than that due to variation in water nutrients (Tables by Generalized Linear models (GLM) based on a quasibinomial dis- tribution and logit-link functions (Crawley, 1993). Lifetime fecun- dity and realised fecundity were analysed using GLM with Poisson distribution and log-link function. Longevity of males and females (data was log transformed) were compared using the Cox Proportional Hazard Model (Cox, 1972; Collett, 1994), using the function coxph (Survival package). Significant results at p < 0.05 were followed by the use of Tukey’s honest significant dif- ference test (a = 0.05) for pairwise comparisons using the Agricolae package (Mendiburu, 2015).

3. Results

Tables 1 and 2 show the means of fitness traits in regard Fig. 1. Lifetime fecundity (number of eggs laid) of E. catarinensis females maintained on plants grown at three nutrient levels (eutrophic ‘‘high”, mesotrophic to the main factors, temperature and nutrient level, independently. ‘‘medium” and oligotrophic ‘‘low”) combined with three constant temperatures (20, Figs. 1–4 show the responses of the insects in all the 25 and 30 °C). Data are presented as mean ± SE. Different letters indicate significant treatments. differences among different treatments (Post hoc pair-wise tests, a = 0.05). 86 M. Ismail et al. / Biological Control 106 (2017) 83–88

1, 2). Lifetime fecundity decreased around 60% with increasing plants grown under oligotrophic levels, (Table 2). The interaction temperature from 20 °Cto30°C, whereas the reduction in fecun- between the two factors was significant (F4, 92 = 11.90; P < 0.001; dity in response to decreasing nutrient levels was around 33% from Fig. 3A). At the highest temperature (30 °C) there were also differ- eutrophic to oligotrophic conditions. Similar reductions were ences in survivorship of insects on plants grown under different found in the other fitness traits (Tables 1, 2). nutrient conditions, with survivorship lowest on low-nutrient plants (Fig. 3A). 3.2. Egg hatching 3.4. Realised fecundity Significantly fewer eggs hatched at 30 °C than at the lower tem- The numbers of offspring that successfully reached the adult peratures (F2, 94 = 31.12; P < 0.001; Table 1), but nutrient level of plant had no impact on egg hatching (F = 2.62; P = 0.07; stage varied almost 10-fold between treatments (Fig. 3B). The 2, 94 ° Table 2). No interaction was found between the two factors highest number of adult offspring was at 20 C(Table 1). Their numbers declined significantly with increasing temperature (F4, 94 = 1.09; P = 0.37; Fig. 2). 2 (v Á2 = 718.97; P < 0.001) (Table 1). With regard to nutrient levels, the highest numbers of adult offspring were produced at high and 3.3. Nymphal survival medium nutrient levels compared to low nutrient levels (Table 2). 2 This was a significant impact (v Á2 = 58.13; P < 0.001). The interac- Almost all of the nymphs reached adulthood at the low and tion between temperature and nutrient levels was also significant 2 intermediate temperatures, but survival of immatures declined (v Á4 = 124.34; P < 0.001) (Fig. 3B). significantly at the highest temperature (F2, 92 = 25.34; P < 0.001; Table 1). Nymphal survival decreased significantly with decreasing nutrient levels (F2, 92 = 3.82; P = 0.02). Overall, survival was higher on plants grown under eutrophic and mesotrophic levels than on

Fig. 2. Egg hatching (percentage ± SE) of E. catarinensis maintained on plants grown at three nutrient levels combined with three constant temperatures. Different letters represent significant differences among three temperatures (p < 0.05).

Fig. 3. (A) Nymphal survival (percentage ± SE) and (B) realised fecundity (mean ± Fig. 4. Male and female longevity (days) for each treatment (H20 = eutrophic at SE) of E. catarinensis females on plants grown at three nutrient levels combined with 20 °C, H25 = eutrophic at 25 °C, H30 = eutrophic at 30 °C; M20 = mesotrophic at three constant temperatures. Different letters indicate significant differences 20 °C, M25 = mesotrophic at 25 °C, M30 = mesotrophic at 30 °C; L20 = oligotrophic among the treatments (Post hoc pair-wise tests, a = 0.05). at 20 °C, L25 = oligotrophic at 25 °C and L30 = oligotrophic at 30 °C). M. Ismail et al. / Biological Control 106 (2017) 83–88 87

3.5. Adult offspring sex ratios (rate of females) Gutbrodt et al., 2012). At 25 °C the relationship conformed to a lin- ear response, where the number of eggs increased with increasing Offspring sex ratios varied marginally in some treatments plant quality. Interestingly, at 30 °C the response became non- (M30 = 0.49 ± 0.06 and L25 = 0.51 ± 0.02) compared to the linear again; the number of eggs and adults in plants grown in others (H20 = 0.54 ± 0.02, H25 = 0.54 ± 0.01, H30 = 0.54 ± 0.03, eutrophic and mesotrophic water were equal, and higher than in M20 = 0.53 ± 0.01, M25 = 0.53 ± 0.02, L20 = 0.54 ± 0.01 and L30 = plants grown in oligotrophic water. Sex ratio plays a large role in 0.56 ± 0.08%), but did not differ significantly with temperature shaping the population dynamic. It can determine the success of

(F2, 91 = 0.12; P = 0.89; Table 1) or nutrient levels (F2, 91 = 1.23; a biological control program, particularly in diploid species such p = 0.29; Table 2). There was also no significant interaction as E. catarinensis, where females need to mate regularly in order between the two factors (F4, 91 = 0.64; P = 0.63). to lay eggs (personal observation). Unlike Craig et al. (1992),we found that there was no impact on the number of female progeny due to the nutrient levels of the water, the temperature or the com- 3.6. Longevity bination of the two factors. In conclusion, our study demonstrated that reproduction of E. Adult males and females survived on average for up to 75 days catarinensis was most effective on plants grown in water with at 20 °C(Fig. 4) but the longevity of both sexes decreased signifi- 2 eutrophic and mesotrophic nutrient levels, at 20 and 25 °C, and cantly with increasing temperatures (Females: v Á2 = 96.95; 2 not as effective on plants in oligotrophic water, particularly at P < 0.001, Table 1), (Males: v Á2 = 122.09; P < 0.001, Table 1). The 30 °C. The majority of reservoirs and impoundments in South nutrient status of the plants had a significant impact on female 2 Africa are nutrient enriched (van Ginkel et al., 2000; Oberholster longevity (v Á2 = 6.31; P = 0.04; Table 2), but no impact on male 2 and Ashton, 2008). This would favour the abundance and quality longevity (v Á2 = 4.16; P = 0.12; Table 2). There was no significant of E. crassipes, and consequently have an indirect positive impact interaction between temperature and nutrient level in the longev- 2 2 on the fitness of E. catarinensis, particularly in temperate areas. ity of either sex (Females: v Á4 = 3.65; P = 0.46; Males: v Á4 = 8.76; Being able to predict the potential impact of the interaction of tem- P = 0.07) (Fig. 4). perature and nutrient level on the fitness of individuals may assist ecologists regarding choice as well as management of biocontrol 4. Discussion agents. In temperate areas we would anticipate successful estab- lishment of E. catarinensis, and a possible subsequent negative In this study we present the first evidence of the impact of the impact on the E. crassipes. In response to results from this study, interaction between temperature and nutrient levels on insect her- we would advise that in warmer areas where temperatures regu- bivores, by demonstrating the effect on some of the fitness traits of larly reach 30 °C the fitness of the biocontrol agent would be the bug E. catarinensis. The significant decrease in fecundity, nym- reduced, and thus more regular re-release of biocontrol agents phal survival and thus in the realized fecundity, was linked to the may be necessitated. higher temperature combined with oligotrophic nutrient levels. The decrease in the realized fecundity might be anticipated due Conflict of interest to the sensitivities of incomplete instars to temperature and plant quality. Consistent with other studies (Diamond and Kingsolver, The authors declare that they have no conflict of interest. 2010; Bauerfeind and Fischer, 2013a), our results showed that the negative impact on insect performance as a consequence of feeding on low quality plants was much more obvious at higher Acknowledgments temperatures (Figs. 1, 3b). Thus we demonstrated that plant qual- ity plays a significant role in tolerance of insects to higher temper- This study was supported by funding from Rhodes University atures. This concurs with findings that plant quality can be a (South Africa), as well as the South African Research Chairs Initia- determinant for the responses of populations to climate variability tive of the Department of Science and Technology, and the National (Buckley and Kingsolver, 2012; Kleynhans et al., 2014). Research Foundation of South Africa. 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