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Nov 8, 2011 - from polyurethane foam common in consumer products. Michael O. Gaylor a,* ..... tudinal fractionation studies (Ter Schure et al., 2002). Crickets ...
Chemosphere 86 (2012) 500–505

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House crickets can accumulate polybrominated diphenyl ethers (PBDEs) directly from polyurethane foam common in consumer products Michael O. Gaylor a,⇑, Ellen Harvey b, Robert C. Hale b a

Departments of Chemistry, Biology and Environmental Science, Davis and Elkins College, 100 Campus Drive, Elkins, WV 26241, USA Department of Environmental and Aquatic Animal Health, School of Marine Science, Virginia Institute of Marine Science (VIMS), The College of William and Mary, P.O. Box 1346, Gloucester Point, VA 23062, USA

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a r t i c l e

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Article history: Received 5 August 2011 Received in revised form 1 October 2011 Accepted 9 October 2011 Available online 8 November 2011 Keywords: Polybrominated diphenyl ethers (PBDEs) Brominated flame retardants (BFRs) Crickets Insects Bioaccumulation Polyurethane foam

a b s t r a c t Polybrominated diphenyl ether (PBDE) flame retardants are added at percent levels to many polymers and textiles abundant in human spaces and vehicles, wherein they have been long assumed to be tightly sequestered. However, the mg kg 1 burdens recently detected in indoor dust testify to substantial releases. The bulk of released PBDEs remain in the terrestrial environment, yet comparatively little research focuses on this compartment. There, insects/arthropods, such as crickets, are the most abundant invertebrate organisms and facilitate the trophic transfer of contaminants by breaking down complex organic matter (including discarded polymers) and serving as food for other organisms. Our experiments revealed that house crickets (Acheta domesticus) provided uncontaminated food and free access to PUF containing Penta-BDE (8.7% dry wt) for 28 d accumulated substantial PBDE body burdens. Crickets allowed to depurate gut contents exhibited whole body burdens of up to 13.4 mg kg 1 lipid RPentaBDE, 1000-fold higher than typically reported in humans. Non-depurated crickets and molted exoskeletons incurred even higher RPenta-BDE, up to 80.6 and 63.3 mg kg 1 lipid, respectively. Congener patterns of whole crickets and molts resembled those of PUF and the commercial Penta-BDE formulation, DE-71, indicative of minimal discrimination or biotransformation. Accumulation factor (AF) calculations were hampered by uncertainties in determining actual PUF ingestion. However, estimated AFs were low, in the range of 10 4–10 3, suggesting that polymer–PBDE interactions limited uptake. Nonetheless, results indicate that substantial PBDE burdens may be incurred by insects in contact with current-use and derelict treated polymers within human spaces and solid waste disposal sites (e.g. landfills, automotive dumps, etc.). Once ingested, even burdens not absorbed across the gut wall may be dispersed within proximate terrestrial food webs via the insect’s movements and/or predation. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Concerns have increased about the accumulation of plastics in the environment. In 2009 alone, 28 million tons of plastics entered the US environment via municipal solid waste (US EPA, http:// www.epa.gov/osw/nonhaz/municipal/msw99.htm). In addition, immense ‘‘garbage patches’’ have been discovered in the major oceanic gyres (Rios et al., 2010). With respect to biological impacts, greatest attention has focused on physical entanglement or digestive blockages due to ingestion of discarded plastics by mammals and birds (Ryan et al., 1988). Hydrophobic plastics can also concentrate persistent organic pollutants (POPs) from ambient air and water and the toxicological implications of these sorbed residues have received recent scrutiny (Teuten et al., 2007, 2009; Rios et al., 2010). However, their levels are orders of magnitude lower than those of intentional polymer additives. ⇑ Corresponding author. Tel.: +1 304 637 1219; fax: +1 304 637 1218. E-mail address: [email protected] (M.O. Gaylor). 0045-6535/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.chemosphere.2011.10.014

Polybrominated diphenyl ethers (PBDEs) have been widely used to flame retard consumer plastics. Of the three commercial PBDE mixtures, Penta-BDE is the most bioaccumulative and toxic and has been listed as a POP under the Stockholm Convention (http:// chm.pops.int/default.aspx). Penta-BDE has been used primarily to flame retard polyurethane foam (PUF) products. About 5.5  108 kg of PUF is produced annually for furniture cushioning in the US (Alliance for Flexible Polyurethane Foam, 2011). Another 2.3  108 kg is used for carpet underlayment in the automotive sector and in other applications (Alcock et al., 2003; Polyurethane Foam Association, 2011). After usage, most PUF products end up in landfills and automotive dumpsites, etc. PUF products are also illegally discarded alongside roads and highways in some rural environments (Matthews County, VA Board of Supervisors Personal Communication). Soil insect abundance and activity is typically high in such waste disposal environments (Robinson, 2005) increasing opportunities for interaction with derelict consumer products and exposure to chemical additives therein. US manufacturers have added percent levels of Penta-BDE to PUF to meet state-mandated

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flame retardancy standards. As PBDEs were not chemically reacted with the polymer, some escaped over the product’s lifetime. The observation of mg kg 1 levels of PBDEs in indoor dust and increasing levels in humans and wildlife underscore the need for a better understanding of the role of polymer products in exposure. In the face of increasing environmental and human health concerns, The European Union officially banned Penta-BDE in 2004, although some member states had already terminated usage and US production ceased at the end of that same year (Frederiksen et al., 2009). Nonetheless, vast amounts persist in current-use and discarded products. While viewed as persistent in the environment, plastics eventually weather and disintegrate (Browne et al., 2008; Barnes et al., 2009). Some PUF formulations are especially vulnerable, crumbling after only a few weeks of exposure to outdoor conditions (Hale et al., 2001). As particle size decreases, surface area increases and so to does the potential for additive PBDE release and dispersal. The importance of finished products rather than manufacturing as a source of PBDEs to the environment was highlighted in a recent Antarctic study (Hale et al., 2008). While no BFR or plastics manufacturing occurs on that continent, substantial PBDE concentrations were discovered in indoor dust within buildings, wastewater treatment sewage sludge and nearby aquatic organisms and sediments. Legacy POPs (e.g. PCBs) were historically released primarily through industrial or heavy commercial processes. Human exposure to such POPs has since occurred predominantly via consumption of contaminated fish, rather than direct contact with PCBcontaining products (Harrad and Diamond, 2006). In contrast, the dominant pathway for human PBDE exposure appears to be ingestion of dust originating from PBDE-treated polymer products in homes, vehicles and the workplace (Harrad and Diamond, 2006; Allen et al., 2008; Frederiksen et al., 2009). Some of the PBDEs within such dust are still contained within polymer fragments (Webster et al., 2009) and this may control their bioavailability and future dispersal and persistence. Owing to extensive usage in polymer products and their ubiquity within human living spaces, losses from in-use and discarded products will remain important PBDE sources to the global environment well into the future (Frederiksen et al., 2009). Alcock et al. (2003) estimated that the total reservoir of BDE 47 alone available for redistribution from finished PUF products to the US and UK environments was about 2620 and 520 metric tons, respectively. This congener constitutes only about 40% of Penta-BDE commercial mixtures (La Guardia et al., 2006). Hence, the total amount of Penta-BDE in play would be more than double these estimates. Fugacity modeling indicates that most polymer products and associated PBDEs will be discharged to, and remain in, the terrestrial environment (Palm et al., 2002). In addition, many insects (e.g. crickets, carpet beetles, silverfish, termites, ants and moth larvae) are prodigious shredders and degraders of natural and synthetic polymers (Robinson, 2005). Many of these are also prolific within solid waste disposal sites and are frequent invaders of human habitations wherein they may cause substantial damage. Nonetheless, most insect-related POP studies to date have focused on aquatic rather than terrestrial species. Recent studies of the role of spiders in transferring aquatic-derived mercury and PCB burdens to birds highlight the potential importance of terrestrial invertebrate transport pathways (Cristol et al., 2008; Walters et al., 2010). Findings of substantial burdens of highly brominated PBDEs in terrestrial-feeding birds of prey (Chen and Hale, 2010) also support the need for further investigation of such exposure routes. Insects constitute a significant fraction of the total species and biomass present in soil-associated ecosystems. Yet we are aware of only three publications addressing PBDE burdens in terrestrial insects (Hale et al., 2002; Wu et al., 2009; Yu et al.,

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2011). In these studies, PBDE measurements were ancillary to the major study foci. Impacts of soil-associated PCBs on the house cricket, A. domesticus (Paine et al., 1993), as well as the utility of this species to serve as a bioindicator of POP contamination in general (Walton, 1989; Paine et al., 1993), have been demonstrated. Such studies indicate that crickets can accumulate and transfer POPs within food webs. Yet, the extent to which such insects may assimilate PBDEs directly from treated polymers has remained virtually uninvestigated. We therefore examined the potential for uptake of Penta-BDE by house crickets allowed access to a commercially treated PUF polymer product. 2. Materials and methods 2.1. Cricket-PUF bioassay The ASTM soil toxicity/bioaccumulation bioassay (ASTM E1676, 1997) was used as a model to assess the accumulation and bioavailability of Penta-BDE contained in commercial PUF to house crickets (A. domesticus). Briefly, 21-d nymphs (Fluker Farms; Port Allen, LA) were acclimated to laboratory conditions for 48 h prior to exposure. Nymphs (n = 10) were randomly assigned to 2 L beakers (N = 4 treatments and N = 4 controls). Food and water (Fluker Farms Cricket QuencherÓ and Cricket FeedÓ) were provided ad libitum. Cylindrical PUF cores (0.5 g; 6 cm  2 cm o.d.) were cut from a large piece of stock furniture foam (1 m2) purchased new from a local upholstery retail shop. Cores and cardboard shelters were placed in the test beakers. Cores were weighed before and after exposure to estimate PUF ingestion. Crickets in control beakers were treated identically, except with no access to PUF. The bioassay was conducted at 26 ± 3 °C, relative humidity of 45 ± 5%, with a 12:12 light:dark photoperiod. Control and PUF-exposed crickets were collected at day 14 and 28 of the experiment. Crickets were depurated by removing the PUF from treatment beakers, while maintaining access to fortified food and water ad libitum for an additional 96 h. Cricket body lengths were measured. Exoskeleton molts were collected as discovered from 14 d- and 28 d-exposed crickets. Owing to the small size of the sheds ( 0.05; ANOVA). Exposure time

Depurated crickets

Non-depurated crickets

Control crickets

Non-exposed moltsa

14 d 28 d

11.1 ± 0.7 10.8 ± 1.5

10.8 ± 1.6 10.9 ± 0.9

10.6 ± 1.3 10.2 ± 1.1

10.3 ± 0.7 9.5 ± 0.8

a Molts were collected and composited (n = 3) as shed from non-exposed crickets of the same age cohort from the stock population reared along with exposed and control crickets.

Fig. 2. Mean contributions of major Penta-BDE constituent congeners in 28 d depurated and non-depurated cricket treatments (N = 4 pools per treatment; n = 10 crickets per pool), molts from PUF-exposed crickets, commercial PUF (n = 4) and DE-71 (data from La Guardia et al., 2006). Error bars represent standard deviations from the means for cricket tissues and PUF. For molts, error bars are the range of the measurements determined for composite molts collected as discovered from 14 d and 28 d treatments.

BDE 47/99 ratio was statistically different (p < 0.05). This may be due in part to faster elimination of BDE 99 with time as previously reported in exposed aquatic invertebrates (Ciparis and Hale, 2005). The BDE 47/99 ratio in crickets examined by Hale et al. (2002), also lab-exposed to Penta-BDE-treated PUF, was similar to those observed here. Comparable congener patterns were also observed in earthworms (Eisenia fetida) exposed to PUF-amended soil in the lab (Gaylor, 2010). However, in a field study of soil invertebrates exposed to PBDEs via land-applied sewage sludges, BDE 47/99 ratios in field crickets ranged from 0.19 to 0.37 and were lower than those calculated for soil and for all other species examined (Gaylor, 2010). This may be explained by differences in exposure substrate and PBDE concentration/partitioning, as well as differences in food sources in field-compared to our lab-exposed crickets.

3.3. PUF ingestion/retention and PBDE bioaccessibility We expected PUF ingestion by crickets to be higher at 28 d than 14 d. However, measured mass losses from the PUF cores (as a surrogate for PUF ingestion) were 7.3 ± 2.1 and 5.7 ± 4.2 mg in 14 d and 28 d depurated treatments, respectively, and 11.4 ± 5.3 and 10.4 ± 4.9 mg in 14 d and 28 d non-depurated treatments, respectively. Measured PUF mass losses were not significantly different and represented only about 1.5–2.3% of the total mass of exposure PUF. This is equivalent to a nominal RPBDE intake of about 1240– 1900 mg. If our estimates accurately represented PUF ingestion, we would anticipate higher total RPBDE body burdens. Thus, our estimates are likely an upper bound estimate of the actual mass of PUF ingested by exposed crickets. Discrepancies between the mass actually ingested and our estimates may be due to: (1) sloppy feeding: shredding insects, such as crickets, may not ingest all fragments separated from the original food/foam item (Clifford and Woodring, 1990); (2) fouling of the PUF: adherence of foreign matter might have increased the apparent weight of the PUF core; (3) reduction of PUF intake due to impacts on digestive processes, i.e. blockage or hunger satiation, as has been suggested for birds

ingesting plastics (Auman et al., 1997). However, as extractable lipid content was similar in PUF-exposed and control crickets (Table 1), the latter seems unlikely. A cessation in PUF ingestion might also explain why tissue RPBDE burdens were unchanged with exposure time in depurated crickets. In 28 d non-depurated crickets apparent PUF ingestion was not proportional to the higher whole body burdens measured. As noted, this may be explained by retention of PBDE-laden PUF fragments in the gut. We were unable to locate any published data on retention of plastics in the gut of Gryllidae or other insect taxa. However, longer gut retention in grasshoppers (Orthoptera: Acrididae) has been reported to enhance extraction of food constituents (Yang and Joern, 1994) and substantial gut retention of plastics in other wildlife taxa has been observed. For example, Ryan and Jackson (1987) estimated a half-life of plastic particulates in the digestive tract of seabirds in excess of one year. After normalizing for the PUF mass loss from the exposure cores, estimated cricket/PUF AFs were low, on the order of 10 3–10 4 for depurated and non-depurated crickets (Table 2). This was not surprising, as release of additives from polymers will be controlled by their rate of diffusivity through the polymer matrix, as well as the distance that must be traveled (Figge and Freytag, 1984). Further, polymers such as PUF effectively retain organic contaminants such as PBDEs and indeed are now the collection media of choice for environmental samplers (Shoieb and Harner, 2002). POPs incurred in other environmental solids such as sediments are assumed to be sorbed to complex pools of natural organic carbon accreted on particles and thereby less accessible to biota. Teuten et al. (2007) reported phenanthrene Kd values of 19 and 135 for sandy and silty aquatic sediment, respectively, but 38,100 for polyethylene powder. However, on an organic carbon basis, partition coefficient (Koc) values were within a factor of five. Naturally occurring organic carbon also occurs at relatively low levels in soil and sediments (i.e. 2–5% w/w basis). In contrast, the TOC of our exposure PUF was 61 ± 6% (n = 4). However, owing to its open-cell structure, the high surface area of PUF should accelerate additive release compared to denser thermoplastics. Shredding of the PUF by insects might further increase polymer surface area and bioaccessibility of additives (see Appendix A for supplemental discussion). Humans spend about 80% of their lives indoors, in close proximity to flame retarded polymer products. The observed cricket PBDE concentrations are about 1000-fold higher than those typically reported for human sera (Frederiksen et al., 2009). Our data suggest that insects frequenting human spaces or contacting discarded PUF products in landfills and other waste disposal sites (e.g. automotive salvage yards) may ingest small amounts of the polymer. These small amounts could, in turn, convey large amounts of PBDEs into associated food webs, regardless of the assimilation efficiency within the prey organism. We are unaware of any studies

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Table 2 Calculated mean (%RSD) cricket/PUF PBDE accumulation factors (AFs) (10 4) for depurated and non-depurated crickets allowed access to PBDE-containing PUF. AFs were computed as the ratio of lipid-normalized tissue PBDE burdens to TOC-normalized PUF PBDE concentrations and then normalized for PUF mass lost (as a surrogate for PUF mass ingested). %RSD = percent relative standard deviations from treatment means (N = 4). PBDEs

Depurated crickets 14 d (10

47 100 99 154 153 RPBDE

5.3 8.0 6.7 17.1 24.3 7.6

4

)

Non-depurated crickets %RSD

28 d (10

24 10 30 29.1 19.3 17

4.1 4.3 6.4 4.2 4.7 5.3

4

)

examining ingestion/absorption of synthetic polymer additives by insects. However, with regards to digestive physiology in A. domesticus, Teo and Woodring (1985) observed gut pH to vary from 4.1 to 7.7 depending upon compartment and feeding regimen. PUF is resistant to degradation within this pH range in vitro. However, Lepom et al. (2010) found that PBDEs were quantitatively extracted from contaminated house dust using synthetic digestive fluids. Similarly, Wang et al. (1997) reported that synthesized poly(ester)urea–urethane PUF was effectively biodegraded in an artificial digestive system via incubation with cholesterol esterase. Saido et al. (2009) recently reported that polystyrene might be degraded in the ocean relatively rapidly, thereby releasing potentially toxic polymer constituents. In their study, a low temperature polyethylene glycol extraction procedure was used and resulting products compared to chemical constituents observed in the environment. However, release of xenobiotic chemicals from polymer particulates into gut fluids may not translate directly into increased bioaccumulation. For example, in modeling organic chemical uptake from soil by earthworms, Jager et al. (2003) concluded that, though digestive fluids increased dissolved concentrations in the gut, they did not alter the fugacity gradient of the chemical. Commercial PUF used in upholstered furniture and automobile cushioning is commonly derived from polyether precursors (Beyler and Hirschler, 1995) and may be susceptible to degradation by a variety of microorganisms (Ghazali et al., 2005). Minute PUF fragments may also be able to cross the gut wall intact, thereby increasing PBDE uptake into tissues. For example, Browne et al. (2008) found that plastic microparticles (9.6 lm maximum particle size) ingested by filter-feeding mussels (Mytilus edulis) accumulated in the haemolymph and persisted there for up to 48 d.

%RSD

14 d (10

22 27 24 28 5.0 28

4.0 4.1 4.2 4.2 5.8 4.1

4

)

%RSD

28 d (10

25 16 20 13 8.3 20

34.6 27.3 36.6 19.2 25.7 31.9

4

)

%RSD 8.10 17.1 25.9 7.60 6.50 14.4

BDE-100, composite molt congener patterns were comparable to whole body crickets, PUF and DE-71 (Fig. 2). For comparison of accumulation, we calculated molt/PUF AFs as the ratio of lipid-normalized molt PBDE burdens to TOC-normalized PBDE concentrations in the estimated PUF mass ingested. After log-transformation, these values were poorly correlated (r2 = 0.35; p > 0.24) with published (Braekevelt et al., 2003) octanol–water partition coefficient (log KOW) values. However, lipid-normalized molt PBDE burdens were strongly correlated (r2 = 0.99; p < 0.0002) with TOC-normalized PBDE concentrations in the ingested PUF (data not shown). Some limited outgassing of additive PBDEs from finished polymer products occurs over time. Indeed, Wilford et al. (2003) examined vapor phase desorption from PBDE-treated PUF by passing air through PBDE-treated PUF plugs and then trapping the resulting volatilized PBDEs. The original congener pattern in the PBDE-treated PUF (i.e. BDE 99 > 47 > 100 > 153 > 154) differed from that of the sampled air (i.e. BDE 47  99 > 100–28 > 49–17), indicating differential removal of the more volatile congeners. Prevedouros et al. (2004) predicted similar outgassing of BDE 47 from in-use consumer products. Such preferential release and transport has also been invoked as one explanation for congener patterns observed in some indoor dust samples (Hale et al., 2006) and in latitudinal fractionation studies (Ter Schure et al., 2002). Crickets molt 8–10 times during their life cycle (Clifford and Woodring, 1990) and a myriad of organisms prey on these and other soil-dwelling insects (and arthropods), including terrestrial and aquatic birds (Walters et al., 2010). Thus, regardless of accumulation pathway(s), shedding of contaminated cricket molts is likely to further redistribute PBDE burdens within terrestrial ecosystems via direct soil deposition or ingestion by other organisms (including other crickets, as observed by Ghouri and McFarlane (1958) in lab-reared A. domesticus) .

3.4. Cuticle PBDE burdens—a possible additional exposure/transport pathway 4. Conclusions Passive diffusion across the waxy cuticle may be an additional route through which soil arthropods are exposed to lipophilic chemicals. For example, though the exact mechanism was not examined, Paine et al. (1993) observed uptake of PCBs by house crickets reared in cages suspended above field-contaminated soils (mean soil burdens = 1150 lg g 1 dw). Exposed crickets accumulated tissue whole body burdens of 1.6 mg kg 1 ww after only 3 d exposure. In the absence of direct contact with the soil, the authors hypothesized that cricket burdens were derived primarily from gas phase transfer. A similar phenomenon has also been observed for sorption of PBDEs to plant surfaces (Huang et al., 2010). To better understand the potential of the cricket cuticle to accumulate PUF-associated PBDEs, burdens in molted exoskeletons (collected and composited as shed) were also examined. Molt RPBDE burdens (63 ± 13 mg kg 1 lipid) were 4-fold higher than burdens in whole depurated crickets, but lower than those measured in 28 d non-depurated crickets (Table S1). With the exception of

Our results indicate that soil-dwelling insects may ingest PUF present in current-use and derelict consumer products within human spaces and waste disposal sites and accumulate appreciable PBDE burdens. Crickets and other insects/arthropods may therefore be underappreciated vectors of PBDE transfer from consumer products into terrestrial food webs. Though such organisms are likely to differ in their capacity to ingest polymeric materials and accumulate PBDEs, future risk assessments should be more inclusive of their role.

Acknowledgments We thank VIMS Analytical Services Center for elemental analysis and Chemtura Corporation for provision of the DE-71 mixture. This is VIMS Contribution #XXXX.

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