MARGARET ENG

I am interested in how exposure to stressors at critical life stages can alter fitness in wildlife.

More specifically, my main interests
are in Ecotoxicology, and how environmental contaminants can perturbgene expression, physiology, neuroanatomy, behaviour, and life historytraits in birds. To answer these questions, I use integrative laboratory and field approaches in novel ways to causally link exposure with effects.

Education and Training
PDF: Toxicology Centre, University of Saskatchewan, Saskatoon, SK (2016 – present)
PDF: Ecotoxicology and Wildlife Health Division, Env. and Climate Change Canada, Delta, BC (2013 – 2016)
PhD: Biological Sciences, Simon Fraser University, Burnaby, BC (2013)
MSc: Biology, York University, Toronto, ON (2007)
BSc (Hons): Biology, University of Victoria, Victoria, BC (2004)

PUBLICATIONS

  • Incubation temperature and PCB-126 exposure interactively impair shorebird embryo and post-hatch development

    Lunny E, Eng ML, Gurney KEB, Morrissey CA. 2020. Env Res 188:109779

    • Abstract

      In oviparous wildlife, many critical physiological and behavioural components are strongly influenced by the embryonic and early post-hatch developmental environment. As such, early life stages in these species are highly vulnerable to both natural and anthropogenic stressors. For example, in birds, incubation temperature may influence the rate of egg development while also affecting contaminant metabolism and absorption in body tissues, resulting in potentially multiplicative impacts on embryonic and posthatch development. We tested the hypothesis that cumulative effects of early contaminant exposure and temperature stress can negatively affect avian development and may have interactive effects that are more detrimental than either stressor individually. Using a controlled egg injection and incubation study on killdeer (Charadrius vociferous), eggs were exposed to a known endocrine disruptor, 3,3′,4,4′,5-pentachlorobiphenyl (PCB-126) and incubated at either low (36 °C), intermediate (37.5 °C), or high (39 °C) temperatures. Our results indicated that eggs incubated at low temperature had earlier detection of heartbeat, longer incubation length, lower growth rate post-hatch, and higher post-hatch mortality, compared to eggs incubated under intermediate temperatures. Higher incubation temperatures resulted in shorter incubation length, earlier detection of heart rate and faster righting time. As predicted, embryo and chick mortality were greater in the PCB-dosed birds incubated at intermediate and high temperatures. Incidence of distended yolk sacs (%) also increased with PCB exposure in all temperature groups, with the largest increase in the high temperature group. Overall, our results show that low incubation temperature can cause greater adverse effects than PCB-126 exposure alone, but that negative effects of PCB-126 exposure are exacerbated by high incubation temperatures. These findings suggest that in natural settings, shorebird embryos may be more susceptible to contaminant exposure when incubated at temperatures either below or above the apparent optimum.

  • In ovo exposure to brominated flame retardants Part I: Assessment of effects of TBBPA-BDBPE on survival, morphometric and physiological endpoints in zebra finches

    Eng ML, Williams TD, Fernie KJ, Renier NK, Henry PF, Letcher RJ, Elliott JE. 2019. Ecotox Env Safety 179:104.

    • Abstract

      Tetrabromobisphenol A bis(2,3-dibromopropyl) ether (TBBPA-BDBPE) is an additive flame retardant used in polyolefins and polymers. It has been detected in biota, including in avian eggs, yet little is known of its effects. We assessed the pattern of TBBPA-BDBPE concentrations in songbird eggs over the incubation period, and the effects of embryonic exposure to TBBPA-BDBPE in a model songbird species, the zebra finch (Taeniopygia guttata). To assess concentrations during embryo development, eggs were injected on the day they were laid with the vehicle control (safflower oil) or 100 ng TBBPA-BDBPE/g egg, and whole egg contents were collected throughout embryonic development on day 0 (unincubated), 5, 10 and 13. To evaluate effects of embryonic exposure to TBBPA-BDBPE, eggs were injected at Hamburger-Hamilton stage 18 (∼80 h after initiation of incubation) with safflower oil only, 10, 50 or 100 ng TBBPA-BDBPE/g egg (albumin injection volume 1 μl/g). Eggs were monitored for hatching success, and nestlings were monitored for growth and survival. At 15 days post-hatch, tissues were collected to assess physiological effects. TBBPA-BDBPE was incorporated into the egg as the embryo developed, and concentrations started declining in late incubation, suggesting biotransformation by the embryo. There were no effects on hatching success, nestling survival, growth, organ somatic indices, or thyroid hormone homeostasis; however, there was evidence that body condition declined in a dose-dependent manner towards the end of the rapid nestling growth phase. This decreased body condition could be a delayed effect of early developmental exposure, or it may be the result of increased exposure to biotransformation products of TBBPA-BDBPE produced over the nestling period, which are predicted to be more bioaccumulative and toxic than the parent compound.

  • In ovo exposure to brominated flame retardants Part II: Assessment of effects of TBBPA-BDBPE and BTBPE on hatching success, morphometric and physiological endpoints in American kestrels

    Eng ML, Karouna‐Renier NK, Henry PF, Letcher RJ, Schultz SL, Bean TG, Peters LE, Palace VP, Williams TD, Elliott JE, Fernie KJ. 2019. Ecotox Environ Safety. 179:151.

    • Abstract

      Tetrabromobisphenol A bis(2,3-dibromopropyl ether) (TBBPA-BDBPE) and 1,2-bis(2,4,6-tribromophenoxy)ethane (BTPBE) are both brominated flame retardants (BFRs) that have been detected in birds; however, their potential biological effects are largely unknown. We assessed the effects of embryonic exposure to TBBPA-BDBPE and BTBPE in a model avian predator, the American kestrel (Falco sparverius). Fertile eggs from a captive population of kestrels were injected on embryonic day 5 (ED5) with a vehicle control or one of three doses within the range of concentrations that have been detected in biota (nominal concentrations of 0, 10, 50 or 100 ng/g egg; measured concentrations 0, 3.0, 13.7 or 33.5 ng TBBPA-BDBPE/g egg and 0, 5.3, 26.8 or 58.1 ng BTBPE/g egg). Eggs were artificially incubated until hatching (ED28), at which point blood and tissues were collected to measure morphological and physiological endpoints, including organ somatic indices, circulating and glandular thyroid hormone concentrations, thyroid gland histology, hepatic deiodinase activity, and markers of oxidative stress. Neither compound had any effects on embryo survival through 90% of the incubation period or on hatching success, body mass, organ size, or oxidative stress of hatchlings. There was evidence of sex-specific effects in the thyroid system responses to the BTBPE exposures, with type 2 deiodinase (D2) activity decreasing at higher doses in female, but not in male hatchlings, suggesting that females may be more sensitive to BTBPE. However, there were no effects of TBBPA-BDBPE on the thyroid system in kestrels. For the BTPBE study, a subset of high-dose eggs was collected throughout the incubation period to measure changes in BTBPE concentrations. There was no decrease in BTBPE over the incubation period, suggesting that BTBPE is slowly metabolized by kestrel embryos throughout their ∼28-d development. These two compounds, therefore, do not appear to be particularly toxic to embryos of the American kestrel.

  • Continuous exposure to mercury during embryogenesis and chick development affects later survival and reproduction of zebra finch (Taeniopygia guttata)

    Heddle C, Elliott JE, Brown TM, Eng ML, Perkins M, Basu N, Wiliams TD. Ecotoxicology

    • Abstract

      Methylmercury (MeHg) is a global environmental contaminant that bioaccumulates and has multiple toxic modes of action. Aquatic species have traditionally been the focus of wildlife toxicological research on mercury, but terrestrial organisms, including passerine birds, can be exposed to similarly elevated levels of MeHg. In this study we exposed a model passerine, the zebra finch (Taeniopygia guttata), to MeHg in ovo, as chicks only, or with a combined ‘in ovo + chick’ treatment. We isolated exposure to specific developmental stages through the use of egg injections (3.2 µg Hg/g egg) and controlled oral dosing of chicks (0.24 µg Hg/g bw/day from day 1 to day 30). In ovo exposure to MeHg reduced hatching success, but there was no effect of MeHg on chick growth. We found that in ovo only or chick only exposure did not have long-term effects, but there was some evidence for longer-term effects of combined ‘in ovo + chick’ exposure on post-fledging survival and potentially sex-biased survival which resulted in very few ‘in ovo + chick’ exposed females surviving to breed. These females also had lower overall breeding productivity that was mainly due to lower hatching success of their offspring, not lower chick-rearing success. We found no effect of treatment on clutch size or latency to laying among females that did lay eggs. Our study suggests that combined embryonic and nestling MeHg exposure has compounding latent effects on productivity, likely through a mechanism that influences the ability of females to lay fertile eggs that hatch.

  • A neonicotinoid insecticide reduces fueling and delays migration in songbirds

    Eng ML, Stutchbury BJM, Morrissey CA. 2019. Science 365:1177.

    • Abstract

      Neonicotinoids are neurotoxic insecticides widely used as seed treatments, but little is known of their effects on migrating birds that forage in agricultural areas. We tracked the migratory movements of imidacloprid-exposed songbirds at a landscape scale using a combination of experimental dosing and automated radio telemetry. Ingestion of field-realistic quantities of imidacloprid (1.2 or 3.9 milligrams per kilogram body mass) by white-crowned sparrows (Zonotrichia leucophrys) during migratory stopover caused a rapid reduction in food consumption, mass, and fat and significantly affected their probability of departure. Birds in the high-dose treatment stayed a median of 3.5 days longer at the site of capture after exposure as compared with controls, likely to regain fuel stores or recover from intoxication. Migration delays can carry over to affect survival and reproduction; thus, these results confirm a link between sublethal pesticide exposure and adverse outcomes for migratory bird populations.

  • Embryonic exposure to environmentally relevant concentrations of a brominated flame retardant reduces the size of song‐control nuclei in a songbird

    Eng ML, Winter V, Elliott JE, MacDougall-Shackleton SA, Williams TD. 2018. Dev Neur 78:799.

    • Abstract

      Environmental contaminants have the potential to act as developmental stressors and impair development of song and the brain of songbirds, but they have been largely unstudied in this context. 2,2′,4,4′,5‐Pentabromodiphenyl ether (BDE‐99) is a brominated flame retardant congener that has demonstrated endocrine disrupting effects, and has pervaded the global environment. We assessed the effects of in ovo exposure to environmentally relevant levels of BDE‐99 on the neuroanatomy of the song‐control system in a model songbird species, the zebra finch (Taeniopygia guttata). Embryos were exposed via egg injection to a vehicle control (DMSO), 10, 100, or 1000 ng BDE‐99/g egg on the day the egg was laid. Chicks were raised to sexual maturity to investigate long‐term effects of BDE‐99 on the adult male brain. Three key song‐control nuclei (Area X, HVC, RA) all showed a dose‐dependent trend toward decreasing volume as BDE‐99 concentration increased, and birds exposed to 1000 ng/g in ovo BDE‐99 had significantly smaller song‐control nuclei volume compared to control birds. High environmental concentrations of BDE‐99 in avian tissues can be within that range and thus could affect development of the song‐control system in birds, and potentially other processes. We previously found that BDE‐99 exposure during the nestling period had no effect of on the song‐control system, although it did have significant effects on some behaviural endpoints. Taken together, these results suggest that exposure to polybrominated diphenyl ether (PBDEs) during critical developmental windows can significantly alter neurological development. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018

  • Part-per-trillion LC-MS/MS determination of neonicotinoids in small volumes of songbird plasma

    Hao C, Eng ML, Sun F, Morrissey CA. 2018. Sci Total Environ 644:1080.

    • Abstract

      Neonicotinoids are the most widely used class of insecticides in the world, and there are increasing concerns about their effects on non-target organisms. Analytical methods to diagnose exposure to neonicotinoids in wildlife are still very limited, particularly for small animals such as songbirds. Blood can be used as a non-lethal sampling matrix, but the sample volume is limited by body size. Neonicotinoids have a low bioaccumulation potential and are rapidly metabolized, therefore, sensitive assays are critically needed to reliably detect their residues in blood samples. We developed an efficient LC-MS/MS method at a part-per-trillion (pg/ml) level to measure eight neonicotinoid related insecticides (acetamiprid, clothianidin, dinotefuran, flonicamid, imidacloprid, nitenpyram, thiacloprid and thiamethoxam) plus one metabolite (6-chloronicotinic acid) in small volumes (50 μL) of avian plasma. The average recovery of target compounds ranged from 95.7 to 101.3%, and relative standard deviations were between 0.82 and 2.13%. We applied the method to screen blood samples from 36 seed-eating songbirds (white-crowned sparrows; Zonotrichia leucophrys) at capture, and detected imidacloprid in 78% (28 of 36), thiamethoxam in 22% (8 of 36), thiacloprid in 11% (4 of 36), and acetamiprid in 11% (4 of 36) of wild-caught sparrows. 6 h after capture, birds were orally dosed with 0 (control), 1.2 or 3.9 mg of imidacloprid/kg bw, test results using this method indicated that plasma imidacloprid was significantly elevated (low 26-times, high 316-times) in exposed groups. This is the first study to confirm neonicotinoid exposure in small free-living songbirds through non-lethal blood sampling, and to demonstrate that environmentally realistic doses significantly elevate circulating imidacloprid concentrations. This sensitive method could be applied to characterize exposure to neonicotinoids in free-living wildlife and in toxicological studies.

  • Ecologically-relevant exposure to methylmercury during early development does not affect adult phenotype in zebra finches (Taeniopygia guttata)

    Morran SAM, Elliott JE, Young J, Eng ML, Basu N, Williams TD. 2018. Ecotoxicology 27:259.

    • Abstract

      Methylmercury causes behavioural and reproductive effects in adult mammals via early developmental exposure. Similar studies in birds are limited and mostly focussed on aquatic systems, but recent work has reported high blood mercury concentrations in terrestrial, passerine songbirds. We used the zebra finch (Taeniopygia guttata) as a model to explore the long-term effects of early developmental exposure to methylmercury exposure. Chicks were dosed orally with either the vehicle control, 0.0315 µg Hg/g bw/day, or 0.075 µg Hg/g bw/day throughout the nestling period (days 1–21 post-hatching). We then measured (a) short-term effects on growth, development, and behaviour (time to self-feeding, neophobia) until 30 days of age (independence), and (b) long-term effects on courtship behaviour and song (males) and reproduction (females) once methylmercury-exposed birds reached sexual maturity (90 days post-hatching). High methylmercury treated birds had mean blood mercury of 0.734 ± 0.163 µg/g at 30 days post-hatching, within the range of values reported for field-sampled songbirds at mercury contaminated sites. However, there were no short-term effects of treatment on growth, development, and behaviour of chicks, and no long-term effects on courtship behaviour and song in males or reproductive performance in females. These results suggest that the nestling period is not a critical window for sensitivity to mercury exposure in zebra finches. Growing nestlings can reduce blood mercury levels through somatic growth and depuration into newly growing feathers, and as a result they might actually be less susceptible compared to adult birds receiving the same level of exposure.