Contaminants in Magnificent Frigatebird Eggs from Barbuda, West

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Marine Pollution Bulletin 75 (2013) 317–321

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Marine Pollution Bulletin

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Baseline Contaminants in magniﬁcent frigatebird eggs from Barbuda, West Indies ⇑ Sarah A. Trefry a, Antony W. Diamond a, Nora C. Spencer b, Mark L. Mallory b, a Atlantic Laboratory for Avian Research, PO Box 4400, University of New Brunswick, Fredericton, NB E3B 5A3, Canada b Biology, Acadia University, Wolfville, NS B3P 2R6, Canada article info abstract

Keywords: We examined persistent organic pollutant and trace element concentrations in eggs of magniﬁcent fri- Seabirds gatebirds (Fregata magniﬁcens), a species of conservation concern breeding in the West Indies. Despite Trace elements that frigatebirds feed at high positions in tropical marine food chains, we detected low levels of most con- Persistent organic pollutants taminants, suggesting limited contamination of their prey. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction elements in eggs of the magnificent frigatebird to provide the first data on contaminant levels in this species, and to assess whether Seabirds are ubiquitous features of oceans, inhabiting all marine contamination should be considered a concern for frigatebirds in areas from the equator to the poles (Schreiber and Burger, 2002). the Caribbean. Because they occupy trophic positions near the top of marine food We collected egg samples in 2010 at a breeding colony of webs, examining seabird reproduction and health is an effective approximately 2000 pairs (Diamond, 1973; Kushlan, 2009) located means by which researchers can monitor the health of marine eco- in coastal mangrove lagoon (primarily Rhizophora mangle and Avi- systems (Furness and Camphuysen, 1997). In particular, many con- cennia germinans) near Codrington, Barbuda (17° 400N, 61° 500W). taminants bioaccumulate and biomagnify in marine food chains Because Codrington Lagoon has been recently designated as a Na- (e.g. Borgå et al., 2001), and consequently seabirds often contain tional Park and out of conservation concern, we gathered only eggs high levels of these contaminants in their tissues (e.g. Braune that were abandoned at the nest site. Eggs were taken from the et al., 2002; Helgason et al., 2008), in some cases at levels that field, returned to Canada whole, and then shipped to the Great can have deleterious effects on wildlife health (Verreault et al., Lakes Institute for Environmental Research (GLIER) at the Univer- 2010). sity of Windsor where whole eggs were homogenized and 2g The magnificent frigatebird, Fregata magnificens (Fig. 1), is an of homogenate were used for POP or trace element analyses. Eggs iconic seabird of tropical waters. Feeding on flying fish (Exocoeti- were generally fresh or in early stages of embryo development. dae) and squid (Ommastrephidae), frigatebirds occupy a niche near POP analyses of sample tissues included determination of the top of their food chains (Cherel et al., 2008), and can travel vast chlorobenzenes (RCBz = 1,2,4,5-tetrachlorobenzene, 1,2,3,4-tetra- distances in search of food (Weimerskirch et al., 2006). They are chlorobenzene, pentachlorobenzene and hexachlorobenzene), also a species of strong conservation concern in the Caribbean hexachlorocyclohexanes (RHCH = a-, b-, and c-hexachlorocyclo- Sea, largely due to loss of and disturbance at breeding sites. More- hexane), chlordane-related compounds (RCHLOR = oxychlordane, over, the species appears to have naturally low reproductive suc- trans-chlordane, cis-chlordane, trans-nonachlor, cis-nonachlor and cess (Diamond and Schreiber, 2002). While alterations to heptachlor epoxide), DDT and its metabolites (RDDT = p,p0-DDE, breeding habitats are thought to be the key problem for the spe- p,p0-DDD and p,p0-DDT), mirex, dieldrin, and PCBs (RPCB = 40 cong- cies, there is also evidence of environmental contamination of eners identified according to IUPAC numbers [Ballschmiter and waters near breeding sites (e.g., Sericano et al., 1995; Ross and Zell, 1980]: 17, 18, 20/33, 28, 31, 33, 44, 49, 52, 70, 74, 82, 87, DeLorenzo, 1997; DeGeorges et al., 2010). We are unaware of any 95, 99, 101, 105, 110, 118, 128, 132, 138, 149, 151, 153, 156, 158, investigation of contaminants in this species (Diamond and 170, 171, 177, 180, 187, 183, 191, 194, 195, 201, 205, 206, 208, Schreiber, 2002), although the related great frigatebird (Fregata and 209). minor) exhibited elevated concentrations of some trace elements All samples were analyzed according to CALA-accredited stan- near Hawaii (Burger and Gochfeld, 2000). Thus, we examined the dard operating procedures (Environment Canada, 1989). Chemical levels of persistent organic pollutants (POPs) and selected trace extraction and cleanup of PCBs and organochlorine pesticides followed the procedures of Lazar et al. (1992). Briefly, tissue homogenates were ground and spiked with 1,3,5-tribromobenzene ⇑ Corresponding author. Tel.: +1 902 585 1798; fax: +1 902 585 1059. as a surrogate recovery standard and extracted with 350 mL of E-mail address: [email protected] (M.L. Mallory).

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logger 1 yr later. This technology provides estimated daily, geo- referenced positions of the bird (e.g., Shaffer et al., 2006). We used the daily position of birds from October through January (i.e. the main breeding season; Diamond and Schreiber, 2002) to generate a map of the main foraging area for frigatebirds at this colony, at a time that they are gathering nutrients to form their egg, as well as provisioning young chicks. Among persistent organic pollutants, most of the legacy organic compounds were detected in frigatebird eggs (Table 1), although concentrations of b-HCH and heptachlor epoxide were below detection limits in all five eggs, and only one of four eggs had detectable levels of trans-chlordane, cis-chlordane and dieldrin. Within PCBs, only the congeners 99, 118, 138, 153, 156, 170, 180, 183, 187, 194, 201, and 206 averaged P1% contribution to RPCB, with dominant congeners being PCB153 (35%), 180 (23%), 138 Fig. 1. The magnificent frigatebird, Fregata magnificens, an iconic tropical seabird, at (10%), and 170 (6%). Consequently, the proportional contribution the mangrove nesting site on Barbuda (photo by Geoff Holroyd). of PCB congeners by chlorination group was dominated by hexa- chlorobiphenyls and heptachlorobiphenyls (Fig. 2). Spearman rank correlations among POPs in eggs were all positive, that is, eggs that dichloromethane:hexane (50:50% v/v, OmniSolve-Grade, VWR, ON, had higher concentrations of one POP tended to have higher con- Canada). Cleanup of the sample was performed by gel permeation centrations of all POPs. In particular, eggs that had higher RDDT chromatography followed by activated Florisil (VWR, ON, Canada) also had higher RPCB (Spearman r = 1.0, P = 0.017) and tended to chromatography. Chemical analysis was performed using a Hew- have higher RHCH (rs = 0.9, P = 0.08). Concentrations of RDDT lett–Packard 5890 gas chromatograph with 5973 mass selective were the most variable among the POPs analyzed (Table 1). The detector (GC-MSD) and 7673 autosampler. The column was a RHCH were dominated by a-HCH (50%) and c-HCH (50%). 60 m 0.250 mm 0.1 m DB-5 (Chromatographic Specialties, l We also were able to detect elevated concentrations of selected Brockville, ON). For every batch of five samples injected (as part trace elements in frigatebird eggs (Table 2), but levels of As, Co, Pb, of a larger run of samples), the surrogate standard, PCB standard Ti and V were below detection limits in all eggs, Cd was not de- mixture, organochlorine standard mixture, method blank and in- tected in four eggs, and Cr and Se were not detected in three eggs. house reference tissue also were analyzed. PCBs were quantified Based on data from the two geologgers, we believe that frigate- according to the method described by Drouillard and Norstrom birds at this colony foraged principally within 500 km of their nest (2003). Detection limits ranged from 0.01 to 0.08 ng/g wet wt. site during the breeding season, although foraging trips may depending on the chemical of study. Blanks and reference tissues, extend out 1500 km, generally in waters to the northeast (Fig. 2). quantified during the sample extractions, were in compliance with Consequently, this is where they would have acquired most of the normal quality assurance procedures instituted by GLIER’s their contaminants, in addition to those already stored in their CALA certified organic analytical laboratory. Sample recoveries tissues from year-round foraging. for the surrogate standard averaged 104 ± 4% (mean ± SE). Chemi- In comparison to measures of contaminants in seabird eggs cal concentrations were not recovery corrected. from other regions, levels of POPs in frigatebird eggs were similar For trace elements, samples were also analyzed according to to or lower than those levels in eggs of the least contaminated sea- CALA-accredited standard operating procedures (Environment bird species anywhere in the world (Table 3; note that these values Canada, 1989). Total mercury (Hg) was determined from 1.8 g tis- do not account for differences in trophic levels in food webs). Lev- sue samples digested in 2:1 H SO :HNO acid, purified, and then 2 4 3 els of RDDT and RHCH were particularly low in frigatebirds. The analyzed by atomic absorption spectrometry-cold vapor genera- ratio of p,p’-DDE: RPCB was 0.21, similar to the low ratios found tion using an Atomic Absorption Spectrophotometer (AAS-300; for marine species elsewhere (Table 3 in Bouwman et al., 2008). Varian) and a vapor generation accessory unit (VGA-76; Varian) Similarly, egg concentrations of Hg were relatively low (Table 3); (e.g. Braune et al., 2002). Other trace elements (aluminum – Al, ar- egg Hg was 2 to >1000 times higher in seabirds breeding elsewhere senic – As, cadmium – Cd, cobalt – Co, chromium – Cr, copper – Cu, (e.g. Muñoz Cifuentes et al., 2003; Ikemoto et al., 2005; Braune, iron – Fe, magnesium – Mg, manganese – Mn, nickel – Ni, lead – Pb, 2007; Dittmann et al., 2011). Within North America, egg Hg in selenium – Se, Ti – titanium, vanadium – V and zinc – Zn) were magnificent frigatebirds was in the lower range of values reported determined from a 1.8 g of sample digested with 5 mL 1:1 H SO :- 2 4 in many other species (0.06–7.3 mg/kg ww; Mierzykowski et al., HNO acid, purified, and then analyzed by Inductively Coupled 3 2005; Akearok et al., 2010; Ackerman et al., 2013). Se was found Plasma Optical Emission Spectrophotometry (ICP-OES) (IRIS in few eggs at low concentrations. Most other trace elements in #701776, Thermo Jarrell Ash Corporation) and the sample re- sponse compared against that generated for a standard calibration curve. Quality assurance/quality control procedures included analysis Table 1 of a method blank (purified water), a certified reference tissue Means ± SD and ranges in ng/g wet wt. of POPs in five eggs of magnificent frigatebirds in Barbuda. ND is not detected. (DOLT-2; National Research Council, Canada) and a randomly selected duplicate sample. All QA/QC measures were in compliance Chemical Mean (SD) Range Coefficient of variation (%) with the normal laboratory operating procedures at the time of % Lipid 6.18 ± 1.88 3.43–7.00 30 analysis. Standard detection limits (lg/g dry wt) were: Al – 1.9; RPCB 110.62 ± 58.04 29.82–170.04 52 As – 0.4; Cd – 0.07; Co – 0.08; Cr – 0.20; Cu – 0.32; Hg – 0.0002; RDDT 26.14 ± 30.06 9.35–79.63 115 RCHLOR 1.95 ± 1.63 0.25–4.47 84 Mn – 0.006; Ni – 0.14; Pb – 0.27; Se – 0.59; V – 0.27; Zn – 0.02. Dieldrin 2.92 ND–2.92 At the same time as the collections, we also captured two fri- Mirex 2.83 ± 1.82 1.08–5.46 64 gatebirds at their nest and attached a LAT2500 (Lotek Wireless, RCBz 0.60 ± 0.30 0.31–1.02 50 Inc.) geologger to a wing tag on each individual, and recovered that RHCH 0.42 ± 0.27 0.07–0.75 64 Author's personal copy

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Fig. 2. Location of the study area in the eastern Caribbean. The red line represents the maximum recorded breeding season foraging extent of two frigatebirds, while the orange color represents the core breeding season foraging area.

frigatebirds had RDDT levels in eggs that were approximately 1000X lower than levels associated with reproductive impairment (Blus, 2011), and similarly most of the other organochlorine residues were found at concentrations orders of magnitude lower than even the ‘no effects levels’ determined in experimental studies on other bird species (Elliott and Bishop, 2011; Harris and Elliott, 2011). Among the non-essential trace elements often considered as potential health concerns, Pb and As were not detected, and Cd was detected in few samples, and when present, were at concentrations orders of magnitude lower than levels at which wildlife health concerns arise (Ohlendorf and Heinz, 2011; Wayland and Scheuhammer, 2011). For Hg, egg concentrations were below the range (0.8–5.1 mg/kg wet wt) associated with adverse effects, and generally well below the range shown to have no adverse effects in non-marine birds (Shore et al., 2011). It was unexpected that so many trace elements were undetected, given that in great frigatebirds, most of these trace elements are at elevated levels in feathers (Burger and Gochfeld, 2000). This may reflect differ- Fig. 3. Proportional contribution of PCB congeners by chlorination group in eggs of magnificent frigatebirds. ences in availability of these elements in the regional prey base, and possibly the ability of some of these elements to be seques- tered in feathers compared to eggs. The combination of low Hg Table 2 in eggs (a non-essential element that readily biomagnifies in food Means ± SD and ranges in lg/g dry wt. of trace elements in five eggs of magnificent chains) and low levels of many other trace elements of concern frigatebirds in Barbuda. suggest that trace metal contamination is not an environmental Chemical Mean (SD) Range concern in the marine food web of this region. % Moisture 81.4 ± 1.9 79.9–84.5 PCB congeners in magnificent frigatebirds were dominated by Al 9.61 ± 0.40 9.07–9.89 those found in many other seabird species (Harris and Elliott, Cd 0.10 2011), but notably with a relatively higher proportion of RPCB Cr 0.54 0.35, 0.72 coming from heptachlorobiphenyls (37%) and octachlorobiphenyls Cu 5.24 ± 4.14 1.59–11.52 Mn 0.38 ± 0.13 0.27–0.60 (7%) than has been found in northern seabirds (hepta – 10–24%, Ni 0.24 ± 0.10 0.16–0.93 octa – < 5%; Borgå et al., 2001; Ruus et al., 2002a,b; Mallory Se 0.79 0.69, 0.89 et al., 2005). Muñoz Cifuentes et al. (2003) also found high propor- Zn 10.98 ± 1.74 9.67–14.01 tions (43%) of hepta- and octachlorobiphenyls in eggs of the pe- Hg 0.55 ± 0.16a 0.41–0.83 lagic, pink-footed shearwater eggs (Puffinus creatopus), but lower a 0.102 ± 0.031 mg/kg wet weight. proportions in more coastal species. Similarly, Quinn et al. (2013) recorded higher proportions of hepta- and octachlorobiphenyls in piscivores compared to other birds breeding in South Africa, and frigatebird eggs were lower than levels found in albatross eggs in Cunha et al. (2012) reported greater proportions of these higher the North Pacific (Ikemoto et al., 2005), although Cr (when de- chlorinated PCBs in brown booby (Sula leucogaster) eggs collected tected) and Cu were higher. From the perspective of wildlife health, at offshore compared to nearshore colonies in Brazil. Differences Author's personal copy

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Table 3 Levels of POPs (ng/g ww) and Hg (lg/g ww) reported from marine bird eggs in selected studies elsewhere in the world.

Species Location Year RPCB RDDT Hg RHCH Reference Chroicocephalus maculipennis Chile 1993 170 700 0.08 3.9 1 Larus dominicanus Chile 1993 210 80 0.06 2.5 1 Sterna trudeaui Chile 1993 240 220 0.5 5.0 1 Phalacrocorax brasilianus Chile 1995 150 190 0.15 0 1 Puffinus creatopus Chile 1999 115 160 0.25 3.0 1 Sula leucogaster Brazil (offshore island) 2007 50 10 2 Sula leucogaster Brazil (nearshore islands) 2007 8400 1800 2 Phalacrocorax carbo South Africa 2008–2009 415 3 Anhinga rufa South Africa 2008–2009 250 3 Larus dominicanus South Africa 2004–2005 100 4 Sterna hirundo China 2008 27 457 5 Larus saundersi China 2008 65 1170 5 Uria aalge Norway 2003 336 138 2.0 6 Rissa tridactyla Norway 2003 689 76 0.08 3.2 6 Larus argentatus Norway 2003 1125 274 0.09 3.1 6 Fratercula arctica Norway 2003 629 202 0.10 3.9 7 Sterna paradisaea North Sea 2008–2010 137 12 0.16 7 Hematopus ostralegus North Sea 2008–2010 130 5 >0.1 7 Uria lomvia Arctic Canada 2003 120 103 1.33 11.2 8 Fulmarus glacialis Arctic Canada 2003 167 124 1.41 5.7 8 Rissa tridactyla Arctic Canada 2003 177 43.5 0.82 7.7 8 Cepphus grylle West Greenland 2000 110 45 5.6 9 Larus hyperboreusa Svalbard, Norway 2006 5771 4243 10 Somateria mollissima Sweden 2008 108 20 11 Larus argentatus Sweden 2008 205 20 11 Oceanodroma leucorhoa Pacific coast, Canada 1985 739 725 20 12 Oceanodroma furcata Pacific coast, Canada 1983 3890 1680 50 12 Cerorhinca monocerata Pacific coast, Canada 1985 607 631 18 12 Phalacrocorax auritus Pacific coast, Canada 1985 2920 464 10 12 Phalacrocorax pelagicus Pacific coast, Canada 1985 1840 274 27 12 Larus glaucescens Pacific coast, Canada 1983 780 520 5 12 Synthliboramphus antiquus Pacific coast, Canada 1986 1110 685 184 12 Fregata magnificens Barbuda 2010 110 26 0.10 0.4 This study

1–Muñoz Cifuentes et al. (2003) (estimated from Fig. 3); 2 – Cunha et al. (2012);3–Quinn et al. (2013);4–Bouwman et al. (2008);5–Gao et al. (2009);6–Helgason et al. (2008);7–Dittmann et al. (2011);8–Braune (2007);9–Vorkamp et al. (2004);10–Verboven et al. (2009);11–Carlsson et al. (2011);12–Elliott et al. (1989). a Yolk only.

in the proportional distribution of PCB congeners among species or marine birds of the Caribbean, and thus additional, regional sur- geographic regions may be attributable in part to differential expo- veys for contamination would be warranted. sure and uptake, but also to differential metabolic capabilities for dealing with these chemicals (Fisk et al., 2001; Ruus et al., Acknowledgments 2002a,b). RHCH had undetectable levels of b-HCH and high proportions Many thanks to Sarah Chisholm and Josh Sayers for assistance of a- and c- HCH, counter to many other studies (e.g., Braune, in the field, and to the Barbuda Council, Antigua and Barbuda 2007; Bouwman et al., 2008; Gao et al., 2009). The relatively low National Parks, and the Environmental Awareness Group of Anti- concentrations of RHCH and domination by a- and c- isomers sug- gua for support and permits. Financial support was provided by gest that the residues were derived from recent inputs rather than Environment Canada (CWS), the National Science and Engineering historical usage. We noted high variation in RDDT among the eggs, Research Council, and a University of New Brunswick William S. as has also been observed in other studies (e.g., Gao et al., 2009). Lewis Doctoral Fellowship (to SAT). This study was conducted in Considerable variation in contaminant profiles can be attributable accordance with the guidelines set for the ethical use of animals to age of the organism (older birds typically having higher concen- and research set forth by the Canadian Council on Animal Care trations) and dietary specialization (i.e., some birds might special- Guidelines and Policies at the University of New Brunswick, under ize on feeding higher in food webs) (Blus, 2011). However, we had Protocol 10045. no data on age or diet for the birds in this study, and thus could not assess factors that might explain the variation in levels. References Collectively, the data from magnificent frigatebird eggs from Barbuda had low levels of POPs and toxic trace elements, among Ackerman, J.T., Herzog, M.P., Schwarzbach, S.E., 2013. Methylmercury is the the lowest reported for any marine birds feeding at higher levels predominant form of mercury in bird eggs: a synthesis. Environmental in food webs. Thus, based on the evidence available, it does not ap- Science and Technology 47, 2052–2060. Akearok, J., Hebert, C., Braune, B.M., Mallory, M.L., 2010. Inter- and intraclutch pear that contamination of food webs is a threat in general to variation in egg mercury levels in marine bird species from the Canadian Arctic. breeding frigatebirds in the Caribbean. However, we caution that Science of the Total Environment 408, 836–840. our sample size was small and from a single colony. There are Ballschmiter, K., Zell, M., 1980. Analysis of polychlorinated biphenyls (PCB) by glass capillary gas chromatography. Composition of technical Arochlor- and Clophen- examples of point-source contamination that is readily detected PCB mixtures. Fresenius Z Analytica Chemica 302, 20–31. by monitoring marine birds, showing substantial differences in Blus, L., 2011. DDT, DDD and DDE in birds. In: Beyer, W.N., Meador, J.P. (Eds.), concentrations along the same general coastline (e.g., Cunha Environmental contaminants in biota, second ed. CRC Press, New York, pp. 425–444. et al., 2012). Consequently, we consider our results a suitable base- Borgå, K., Gabrielsen, G.W., Skaare, J.U., 2001. Biomagnification of organochlorines line, but we note that there is a paucity of data on contaminants in along a Barents Sea food chain. Environmental Pollution 113, 187–198. Author's personal copy

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