Effects of Contaminants of Emerging Concern on Myzus Persicae (Sulzer, Hemiptera: Aphididae) Biology and on Their Host Plant, Capsicum Annuum
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UC Irvine UC Irvine Previously Published Works Title Effects of contaminants of emerging concern on Myzus persicae (Sulzer, Hemiptera: Aphididae) biology and on their host plant, Capsicum annuum Permalink https://escholarship.org/uc/item/9pm2w1b9 Journal Environmental Monitoring and Assessment, 190(3) ISSN 0167-6369 1573-2959 Authors Pennington, Marcus Rothman, Jason A Jones, Michael et al. Publication Date 2018-02-08 DOI 10.1007/s10661-018-6503-z Peer reviewed eScholarship.org Powered by the California Digital Library University of California Environ Monit Assess (2018) 190:125 https://doi.org/10.1007/s10661-018-6503-z Effects of contaminants of emerging concern on Myzus persicae (Sulzer, Hemiptera: Aphididae) biology and on their host plant, Capsicum annuum Marcus John Pennington & Jason A. Rothman & Michael Bellinger Jones & Quinn S. McFrederick & Jay Gan & John T. Trumble Received: 13 November 2017 /Accepted: 22 January 2018 # Springer International Publishing AG, part of Springer Nature 2018 Abstract Many countries are utilizing reclaimed waste- differences due to chemical treatments. Plants, however, water for agriculture as water demands due to drought, displayed significant growth reduction in antibiotic and rising temperatures, and expanding human populations. mixture treatments, specifically in wet root masses. Unfortunately, wastewater often contains biologically Antibiotic treatment masses were significantly reduced active, pseudopersistant pharmaceuticals, even after in the total and root wet masses. Mixture treatments treatment. Runoff from agriculture and effluent from displayed an overall reduction in plant root wet mass. wastewater treatment plants also contribute high con- Our results suggest that the use of reclaimed wastewater centrations of pharmaceuticals to the environment. This for crop irrigation would not affect aphid populations, study assessed the effects of common pharmaceuticals but could hinder or delay crop production. on an agricultural pest, the aphid Myzus persicae (Sulzer, Hemiptera: Aphididae). Second instar nymphs Keywords CECs . Microbial communities . Pollution . were transferred to bell peppers (Capsicum annuum) Antibiotics . Wastewater that were grown hydroponically. Treatment plants were spiked with contaminants of emerging concern (CECs) at environmentally relevant concentrations found in Introduction reclaimed wastewater. M. persicae displayed no differ- ences in population growth or microbial community According to the National Center for Health Statistics (2014), there have been increasing pharmaceutical pre- M. J. Pennington : J. Gan : J. T. Trumble scriptions for the past 30 years, and they have almost Graduate Program in Environmental Toxicology, University of tripled in the past 14 years alone (Schumock et al. 2014). California, Riverside, CA 92521, USA For agriculture, in 2013 over 6.6 million kg of the 9.1 M. J. Pennington (*) : J. A. Rothman : M. B. Jones : million kg of antibiotics used were to increase produc- Q. S. McFrederick : J. T. Trumble tion (Department of Health and Human Services 2013). Department of Entomology, University of California, 417 Common Bcontaminants of emerging concern^ (CECs) Entomology Building, Riverside, CA 92521, USA (pharmaceuticals, antibiotics, mental stimulants, and e-mail: [email protected] surfactants) can be excreted by both humans and ani- J. A. Rothman : Q. S. McFrederick mals with little or no change in the chemical structures Graduate Program in Microbiology, University of California, (Hirsch et al. 1999; Ternes et al. 2004; Yamamoto et al. Riverside, CA 92521, USA 2009) and, not surprisingly, they have been appearing in J. Gan wastewater, and in some cases tap water, over the past Department of Environmental Science, University of California, few years (Monteiro and Boxall 2013; Sklerov and Riverside, CA 92521, USA Saucier 2011)(Table1). 125 Page 2 of 11 Environ Monit Assess (2018) 190:125 Table 1 Contaminants of emerging concern (CEC) treatment (Alvarez et al. 2013; Chefetz et al. 2008; Gan et al. group components and concentration 2012;Kinneyetal.2006; Thiele-Bruhn 2003). Contaminant Concentration Reference Our recent studies of the effects of pharmaceuticals (μg/L) on aquatic insects show that at concentrations found in reclaimed water, CECs can alter development of the Antibiotics medically important mosquito Culex quinquefasciatus, Oxytetracycline 72.90 (Kolpin et al. 2002) its susceptibility to a common larvicide, and its larval Lincomycin 0.730 (Kolpin et al. 2002) microbial communities (Pennington et al. 2015, 2016). Ciprofloxacin 6.500 (Mutiyar and Mittal Female Megaselia scalaris, which are ecologically im- 2014) portant detritivores, also displayed an increased devel- Hormones opmental period, which could jeopardize the popula- 0.831 (Kolpin et al. 2002) tion’s survival when exposed to CECs (Pennington 17α- et al., 2017a, b). Also, the common agricultural pest -Ethynylestradiol 17β-Estradiol 0.200 (Kolpin et al. 2002) Trichoplusia ni (cabbage looper) was negatively affect- ed by antibiotics through a plant matrix (Pennington, 19-Norethindrone 0.872 (Kolpin et al. 2002) Rothman, Dudley, et al. 2017). A common birth control Estrone 0.112 (Kolpin et al. 2002) agent, 17α-ethinylestradiol, and Bisphenol-A, a com- Mixture mon plasticizer, have been shown to cause deformities Acetaminophen 10.00 (Kolpin et al. 2002) in the midge Chironomus riparius (Watts et al. 2003). Caffeine 6.000 (Kolpin et al. 2002) However, aquatic insects’ constant exposure to these Antibiotics Concentration CECs is likely greater than most terrestrial insects. In- as above terestingly, many CECs were not designed to specifical- Hormones Concentration as above ly to impact microbes but have been shown to affect microbial communities. For example, the mental stimu- lant caffeine can alter biofilm respiration, and diphen- Most wastewater treatment facilities are not capable hydramine, an antihistamine, has been shown to modify of removing all pharmaceuticals (Gros et al. 2010; the microbial community of lake biofilms (Rosi- Hedgespeth et al. 2012), resulting in these compounds Marshall et al. 2013). Therefore, accurately predicting being found in effluent. In addition, during heavy the consequences of specific CECs, even in model in- storms, untreated wastewater overflow can release even sects, currently is difficult if not impossible. This prob- higher concentrations of some pharmaceuticals, which lem is exacerbated by a general lack of information then directly contaminate the environment (Phillips regarding effects of pharmaceuticals and other CECs et al. 2012). Many of these compounds can be found on the microbial communities of terrestrial insects. at biologically active concentrations in surface waters Arthropods, such as insects and crustaceans, rely on around the world (Alvarez et al. 2013;Fineetal.2003; hormones to grow, develop, mate, and produce pigmen- Huang et al. 2013; Kolpin et al. 2002; Mutiyar and tation (Jindra et al. 2013; Knowles and Carlisle 1956; Mittal 2014; Shappell et al. 2007; Wei et al. 2011). In Martín et al. 2001). However, many pharmaceuticals, addition, there is also an increased effort to use especially mammalian sex hormones, are structurally reclaimed wastewater in drought-affected areas similar to chemicals that these organisms rely on for (Brown et al. 2013;Wuetal.2012), resulting in in- development. These pharmaceuticals bind to receptors creased exposure. In agriculture/livestock operations, and either increase or disable their counterparts’ natural pharmaceuticals are found in manure that is used as function. Endocrine disruption has been noted in birds, fertilizer for feed and crops, effectively compounding reptiles, and arthropods, primarily in the modification of the pharmaceutical concentrations (Kumar et al. 2005; primary and secondary sexual characteristics, and Shappell et al. 2007; Wei et al. 2011). Current research changes in courtship behaviors (Gonzalez et al. 2001; shows that these chemicals tend to be both Hoffmann and Kloas 2012;Jindraetal.2013; Segner pseudopersistant in soil and detrimental to soil microbes et al. 2003; Tompsett et al. 2012, 2013). While most arthropod hormones do not closely match those of mammals, their molting hormone (ecdysone) is very Environ Monit Assess (2018) 190:125 Page 3 of 11 125 similar in structure to the mammalian female sex hor- CECs when translocated through plants to terrestrial mone 17β-estradiol. Increased molting events and inhi- insects, especially those with specialized feeding tech- bition of chitobiase, the enzyme responsible for diges- niques. Depending on the acquisition and sequestration tion of the cuticle during insect molting, have been by their host-plant species, insects with phloem-limited noted in crustaceans exposed to mammalian hormones feeding methods, such as aphids, could have either (Rodríguez et al. 2007; Zou and Fingerman 1997). In reduced or increased exposure to CECs. Because previ- addition to these effects, pharmaceuticals have been ous research demonstrated a substantial change in both shown to have delayed cross-generational effects the biology and microbial communities of other insects (Watts et al. 2001). when treated with ecologically relevant levels of CECs Aphids are phloem-limited hemimetabolous insects (Pennington et al. 2015, 2016; Pennington, Rothman, (immature insects resemble the adults and do not under- Dudley, et al. 2017; Pennington, Rothman, Jones, et al. go complete metamorphosis). Myzus persicae (Sulzer, 2017), and