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Bioaccumulation of persistent halogenated organic pollutants in insects: Common alterations to the pollutant pattern for different insects during metamorphosis Yu Liu, Xiaojun Luo, Li-Qian Huang, Le_Huan Yu, and Bi-Xian Xian Mai Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b00616 • Publication Date (Web): 12 Apr 2018 Downloaded from http://pubs.acs.org on April 12, 2018

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Environmental Science & Technology

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Bioaccumulation of persistent halogenated organic pollutants in insects: Common alterations to the pollutant pattern for different insects during metamorphosis

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Yu Liu, †, ‡ Xiao-Jun Luo, †,* Li-Qian Huang, †, ‡ Le-Huan Yu, § Bi-Xian Mai, †

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ABSTRACT: Few studies have examined the accumulation and fate of persistent

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halogenated organic pollutants (HOPs) in insects. We measured HOPs, including

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dichlorodiphenyltrichloroethanes

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halogenated flame retardants, in insects from four taxonomic groups collected from an

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e-waste site. Dragonfly larvae collected from a pond contained the highest

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concentrations of all chemicals except DDTs, while the litchi stinkbugs contained the

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lowest. Different insect taxa exhibited different contaminant patterns which could be

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attributed to their habitats and feeding strategies. Bioaccumulation factors for

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dragonfly larvae and biomagnification factors for moth and grasshopper larvae were

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significantly positively correlated with the octanol-water partition coefficient of the

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chemicals (log KOW < 8). Common nonlinear correlations between the ratio of larval

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to adult concentrations and log KOW were observed for all taxa studied. The ratio of

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concentrations decreased with increasing values of log KOW (log KOW < 6–6.5), then

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increased (6 < log KOW < 8) and decreased again (log KOW > 8). This result implies

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that the mechanism that regulates organic pollutants in insects during metamorphosis

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is common to all the taxa studied.

†

State Key Laboratory of Organic Geochemistry and Guangdong Key Laboratory of Environmental Resources Utilization and Protection, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, P. R. China. ‡ University of Chinese Academy of Sciences, Beijing 100049, P. R. China. § School of Biology and Food Engineering, Guangdong University of Education, Guangzhou 510303, P. R. China. *

Corresponding author. [email protected]

(DDTs),

polychlorinated

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ACS Paragon Plus Environment

biphenyls,

and


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Table of Contents/ Abstract Art

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INTRODCTION

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Halogenated organic pollutants (HOPs), such as polychlorinated biphenyls (PCBs),

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polybrominated diphenyl ethers (PBDEs), and dichlorodiphenyltrichloroethanes

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(DDTs), are ubiquitous contaminants in the environment. HOPs can accumulate in

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organisms and become magnified along the food chain because of their

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hydrophobicity.1,

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Convention on Persistent Organic Pollutants. In response to these regulations, some

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alternative halogenated flame retardants (HFRs), such as decabromodiphenyl ethane

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(DBDPE) and Dechlorane Plus (DP), are used as replacements in some applications.3

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These alternative HFRs have similar physiochemical properties as PBDEs, and

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available data have revealed that they could also bioaccumulate in wildlife and

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become biomagnified in food webs.4, 5

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DDTs, PCBs, and PBDEs are regulated by the Stockholm

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Insects are a dominant component of biodiversity in both aquatic and terrestrial

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ecosystems, where they play a key role. Insects are an important link between

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primary producers (plants) and secondary consumers, and occupy multiple ecological

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niches in both aquatic and terrestrial food webs because of their biomass and the large

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number of taxonomic groups that exist.6, 7 Thus, insects are the initial step for the

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abundant transportation and bioaccumulation of organic pollutants in the biosphere.8, 9

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For example, aquatic adult insects (e.g., chironomids and mayflies) can export HOPs

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to terrestrial spiders, frogs, and bats that prey on them because the contaminants from

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sediments bioaccumulate in them as larvae and during metamorphosis.10-12 Previous

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research has mostly focused on contaminant transport mechanisms by emergent 3



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aquatic insects; however, terrestrial insects also play an important role in enriching

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and transferring pollutants to insectivores.13, 14

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Metamorphosis is an inevitable stage in the life history of insects.15 This process

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alters the stable isotope signatures and accumulation of HOPs in insects that are the

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regulators of exposure and contaminant flux in food webs because larvae and adults

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are a common diet of different recipient consumers.16-18 The impacts of insect

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metamorphosis on contaminants vary widely.19 For example, polycyclic aromatic

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hydrocarbons (PAHs) are predominantly lost during metamorphosis; in contrast,

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PCBs are retained and concentrated in adults, causing up to a three-fold higher

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concentration in adults and higher exposure risks to their predators.20 Although some

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evidence points to the predictability of the effects of metamorphosis on persistent

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organic pollutant bioaccumulation, no common or synthesis predictive framework

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exists.

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In this study, we collected various insects from four taxonomic groups and three

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types of metamorphosis from an extensive e-waste recycling region in southern China.

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First, carbon and nitrogen stable isotopes were analyzed to identify the food source

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and trophic position of the insects. Second, the levels and congener profiles of the

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HOPs in larval and adult insects, and their food and habitats, were investigated. The

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objective of this study was to elucidate the bioaccumulation characteristic of the

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HOPs in these insects and assess the effect of metamorphosis on HOP accumulation

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patterns. This study is the first report to show that a common mechanism regulates

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organic pollutants in these insects during metamorphosis. 4


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MATERIALS AND METHODS

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Sampling. All the samples were collected around a pond and from surrounding

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regions within a 50 m radius in Longtang Town, Qingyuan County, Guangdong

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Province (Figure S1). The pond has been heavily polluted by chemicals associated

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with e-waste, as a large amount of e-waste was discarded therein. Insects including

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dragonflies, butterflies, moths, grasshoppers (Oxya chinensis), and litchi stinkbugs

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(Tessaratoma papillosa), were collected between September 2015 and November

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2016 in four sampling campaigns. Dragonflies, butterflies, and moths were not

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grouped into single taxon considering that the sample size was too small for each

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species and that the habitat and feeding habit are similar for members of the same

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family. Some of the aquatic dragonfly larvae were taken from the pond and the

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remaining were collected from a ditch in the corn fields near the pond using a

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macro-invertebrate dip net along the bank. Other terrestrial insects were captured

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using sweep nets on trees and fields around the pond. All insect samples were

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identified and divided into larvae and adults. The larval stage for grasshoppers and

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litchi stinkbugs can be recognized by the absence wings or the presence of short wing

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pads. The individual insects were too small to perform contaminant analyses on them;

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they were therefore pooled into a composite sample for each taxon, per sampling

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campaign. Additionally, guava (Psidium guajava) leaves (host plant of moth larvae)

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grass (hosts for grasshoppers), and soil from the fields, and water from the pond, were

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collected for contaminant analysis from the same sites where the insects were

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sampled. A total of 17 abiotic samples and 72 composited biotic samples from 1,549 5



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individuals were obtained. All samples were transported to the laboratory in an ice

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box; they were then freeze-dried, homogenized using a stainless steel blender, and

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stored at -20 °C until analysis. Detailed information about each sample is provided in

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the Supporting Information (SI) and Table S1.

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Sample Preparation. Details on the extraction, cleanup, and quantification of HOPs

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in biotic and abiotic samples had been provided in detail elsewhere;21, 22 thus, only a

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brief description is provided here. After spiking with surrogate standards (PCB24, 82,

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and 198; BDE118; BDE128; 4-F-BDE67; 3-F-BDE153; and 13C-BDE209), 1 g of the

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samples (dry weight) were Soxhlet extracted for 48 h using hexane/dichloromethane

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(1/1, v/v). The extracts were purified using concentrated sulfuric acid and further

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cleaned in a multilayer Florisil silica gel column. The extracts were eluted with

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hexane (45 ml) followed by dichloromethane (50 ml) and were further concentrated

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to near dryness under a gentle nitrogen flow before finally being reconstituted in

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isooctane (100 µL) for analysis. The recovery standards (PCB30, 65, and 204;

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BDE77, 181, 205) were spiked before instrumental analysis. The specific procedures

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for the pretreatment and cleanup of the insect, water, soil, and plant samples, and the

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details of the instrumental analysis, are given in the SI.

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Quality Assurance and Quality Control. Quality assurance and quality control were

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performed by analyzing procedural blanks, triplicate spiked blanks, triplicate spiked

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matrices, and triplicate samples. Procedural blanks were analyzed consistently for

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each batch of nine samples; therefore, the mean values were used for subtraction.

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Trace amounts of PCBs, PBDEs, DP, and DPDBE were detected in the procedure 6


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blanks, but the target hexabromobenzene (HBB), pentabromotoluene (PBT),

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pentabromoethylbenzene (PBEB), polybrominated biphenyls (PBBs), and DDTs were

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not detected. The levels of target chemicals in the blanks were less than 10% of those

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in the samples. The relative standard deviations for all analytes were butterfly and moth > grasshopper > litchi stinkbug (Table 1) for

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both the adult and larval sample datasets. The dragonflies have habitats and feeding

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habits that are completely different from those of the other insects. Dragonflies live in

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aquatic environments as larvae, and they are predators both at that stage and as adults.

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Furthermore, their larval stage can last up to several years, while other three taxa live

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only for several months. This could be the reason for the relatively high contaminant

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levels observed in the dragonflies. The other three taxa are all terrestrial

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phytophagous insects. However, the feeding habit of the litchi stinkbug is different

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from those of grasshoppers, butterflies, and moths. Litchi stinkbugs suck the sap from

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flowering and fruiting shoots of a host plant to obtain their nutrients, while

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grasshoppers and butterfly and moth larvae chew the leaves of a host plant. 11



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Hydrophobic organic pollutants are stored mainly in leaves rather than in sap22; this

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could be contributing to the low levels of contaminants in the litchi stinkbugs.

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The concentrations of PCBs and DDTs in the grasshoppers are one to two orders

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of magnitude lower than those found in the butterflies and moths (Table 1). However,

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the concentrations of HFRs such as PBDEs, DBDPE, and other BFRs in the

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grasshoppers are similar to those in the butterflies and moths. This can be attributed

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to their different host plants. The concentrations of HFRs in the grass are similar to

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those in the guava leaves. However, the concentrations of PCBs and DDTs (52 and

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5.6 ng/g dw, respectively) in guava leaves are 20 times higher than those in grass (2.0

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and 0.3 ng/g dw, respectively) (Table S3).

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The PCB concentrations in grasshoppers and butterflies (7.7–27 ng/g lw) and in

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emerged chironomids and dragonflies (12–24 ng/g lw) collected from effluent

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downstream of a waste treatment plant in China27 are one to two orders of magnitude

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lower than those in the present study. The PCB concentrations in non-predatory,

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predatory, and all terrestrial insects (3–4 ng/g lw, 145 ng/g lw, and 15 ng/g lw,

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respectively) from Lake Hartwell, USA were much lower than those in the present

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study. But the PCB concentrations in chironomids (450–1,850 ng/g lw) from Lake

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Hartwell were comparable with those in the present study.10 The PCB concentrations

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in edible insects (such as the greater wax moth, migratory locust, and mealworm

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beetle) from Belgium varied from 0.027–2.06 ng/g wet weight (ww).28 The highest

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concentration (2.06 ng/g ww) measured there was similar to those in the grasshoppers,

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but lower than those in the dragonflies, butterflies, and moths, in the present study. 12


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The concentrations of PCBs in the dragonflies (530–9,200 ng/g lw) in the present

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study are approximately the same as those in the chironomids (920–9,800 ng/g lw)

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and mayflies (300–5,800 ng/g lw) used as bio-indicators to monitor seriously

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contaminated regions in North America and Europe.19, 29, 30

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The levels of PBDEs in dragonflies, butterflies, and grasshoppers in the present

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study are slightly lower than those in insects from a typical e-waste burning site in

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China (760–1100 ng/g lw).31 However, the median concentration of PBDEs in the

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dragonfly larvae from the pond is several orders of magnitude higher than that found

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in damselfly larvae from sixteen ponds in Flanders, Belgium (0.05). The fanti values in

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the insects are similar to those in their host plants and the abiotic samples, indicating

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that isomer-selective bioaccumulation of DPs does not occur in the insects.

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Bioaccumulation and Biomagnification in Insects. Bioaccumulation factors (BAFs)

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for dragonfly larvae in the pond and biomagnification factors (BMFs) for moth larvae

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were calculated to investigate the influence of the log KOW on the bioaccumulation of

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PCBs and PBDEs in aquatic and terrestrial insects (Table S4 and Figure S8). BMFs

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for grasshopper larvae were only calculated for PCBs since the levels of most of

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PBDE congeners were rather low in both grasshopper larvae and grass, which would

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result in a greater uncertainty. Bioaccumulation in litchi stinkbugs was not calculated

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because data on its food source was not available from the present study. All

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calculations of concentrations were based on the dry weight in the insects; a detailed

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calculation is given in the SI.

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The BAF values in the dragonfly larvae ranged from 910–1,400,000 for

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individual PCB congeners and 7,800–200,000 for individual PBDE congeners. The

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BAF values of ΣPCBs in dragonflies from an urban riparian zone affected by a

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wastewater treatment plant ranged from 71,000–140,000 (small dragonflies and larger

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dragonflies, respectively),27 which were similar to the value found in the present

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study (75,000 for ΣPCBs). The BMF values ranged from 0.25–2.11 for PCBs and 17



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0.47–1.07 for PBDEs in moth larvae and from 0.31–17.2 for PCBs in grasshopper

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larvae (Table S4). The BMFs for ΣPCBs and ΣPBDEs in the moth larvae were 0.78

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and 0.91, respectively. However, the BMF for ΣPCBs in the grasshopper larvae was

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2.19. It is difficult to explain the difference in BMFs for the grasshopper larvae and

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moth larvae. Till date, no BMF data for insects were available; thus, a comparison to

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other results was impossible.

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Significantly positive correlations were found between log BAF (or BMF) and

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log KOW (for log KOW < 8) for all PCB and PBDE congeners, with the exception of

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BDE206 and BDE209 in both aquatic and terrestrial insects (R2 = 0.60–0.84, p

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