Mercury exposure and altered parental nesting behavior in a wild

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Ecotoxicology and Human Environmental Health

Mercury exposure and altered parental nesting behavior in a wild songbird Christopher Alex Hartman, Joshua T Ackerman, and Mark P Herzog Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b07227 • Publication Date (Web): 29 Mar 2019 Downloaded from http://pubs.acs.org on March 30, 2019

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Environmental Science & Technology

Mercury exposure and altered parental nesting behavior in a wild songbird

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C. Alex Hartman*, †, Joshua T. Ackerman†, and Mark P. Herzog†

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†U.S.

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Business Park Drive, Suite D, Dixon, California, 95620, USA

Geological Survey, Western Ecological Research Center, Dixon Field Station, 800

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*Corresponding author; E-mail: [email protected]

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1 ACS Paragon Plus Environment


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ABSTRACT

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Methylmercury is a neurotoxin and endocrine disruptor and may impair avian reproduction

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directly through embryotoxicity or by altering parental care behaviors. We studied mercury

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exposure and incubation behavior of free-living tree swallows (Tachycineta bicolor) nesting in

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artificial nest boxes. Using small temperature dataloggers, we measured incubation constancy

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(the proportion of each day the female spent incubating eggs), the number of incubation recesses

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taken per day, and the duration of incubation recesses. We also assessed maternal mercury

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exposure by measuring mercury concentrations in both blood and eggs. Females with higher

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mercury concentrations exhibited lower incubation constancy, took more frequent and shorter

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incubation recesses, and were more likely to take incubation recesses that caused nest

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temperature decreases that were likely to slow embryonic development. Overall, females that

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laid eggs with the highest observed mercury concentration (0.53 μg/g fww) spent an average of

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12% less time incubating their eggs over the 14-day incubation period than females that laid eggs

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with the lowest mercury concentration (0.07 μg/g fww). Because less time spent incubating can

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lower egg temperatures, slow embryonic development, and potentially lengthen the incubation

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period, these results suggest that environmentally relevant mercury concentrations may

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negatively influence reproduction by altering parental nesting behaviors of wild songbirds.

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INTRODUCTION

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Methylmercury, the persistent and highly toxic form of mercury, is a globally pervasive

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contaminant that can adversely affect wildlife health.1,2 Negative effects of methylmercury on

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avian reproduction are particularly acute, with numerous studies finding elevated methylmercury

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concentrations associated with reduced reproductive performance including lower breeding


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propensity, egg hatchability, nest success, and fledgling success.2,3 Maternal transfer of

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methylmercury to the egg can impair avian reproduction directly through embryotoxicity, and

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greater mortality and developmental malpositions have been observed at higher egg mercury

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concentrations.4–8

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Methylmercury may also impair avian reproduction by altering parental care behaviors of

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adult birds. In birds, parental care, such as incubation, brooding, provisioning of young, and nest

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defense is largely moderated by hormonal mechanisms including gonadal steroids (e.g.,

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progesterone, testosterone), corticosterone, and the pituitary hormone prolactin.9,10

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Methylmercury is a well-known neurotoxin and endocrine disruptor,11,12 and elevated mercury

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concentrations have been associated with lower blood prolactin concentrations13 and deficient

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parental care in birds, including fewer nesting attempts,14 poor nest construction,15 less time

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spent incubating eggs and greater egg neglect,16–18 abnormal incubation and chick provisioning

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behavior,19 and greater likelihood of nest abandonment.20,21 Nest abandonment results in

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complete failure of the nesting effort whereas greater egg neglect and less time spent incubating

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may increase exposure of eggs to temperatures that are suboptimal, and even detrimental, to

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embryonic development. Thus, less time spent incubating can slow embryonic growth and

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development, thereby lengthening the incubation period and increasing exposure risk of nest

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predation.22–24 Furthermore, lower average egg temperatures associated with less time spent

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incubating may reduce the quality (e.g., body mass, size, composition, and growth rate) of

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hatched offspring.24–27

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Despite the role of hormones in moderating parental care and the ability of

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methylmercury to disrupt endocrine function, results of experimental laboratory studies

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investigating whether elevated mercury concentrations alter parental incubation behavior have



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been equivocal. Studies of captive zebra finches (Taeniopygia guttata) have found either no

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effect of methylmercury exposure on nest attendance,15 or that individuals exposed to

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methylmercury spent less time at the nest and were less likely to hatch eggs than those not

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exposed to methylmercury.17 Captive American kestrels (Falco sparverius) exhibited little

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change in incubation performance across a wide range of mercury concentrations, with total

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incubation failure occurring only at very high mercury concentrations.28 Whereas these

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laboratory-dosing studies allowed for experimental manipulation of mercury treatment groups,

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removal of various environmental stressors that wild birds must also endure may have lessened

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the impact of elevated mercury concentrations on incubation behavior. Previous work has shown

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that ambient temperatures and weather conditions can influence songbird incubation behavior,

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including time spent incubating and the number of incubation recesses taken.29–32 Furthermore,

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high ambient temperatures during the nestling period have been associated with reduced

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fledgling production of tree swallows (Tachycineta bicolor) nesting at mercury contaminated

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sites but not at reference sites,33 suggesting that environmental conditions can interact with

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mercury exposure to affect reproduction. Yet, there have been few field studies investigating the

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role of mercury exposure on incubation behavior of wild birds.3,34,35 In one such study of wild

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common loons (Gavia immer), males and females with high mercury concentrations left eggs

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unincubated more often than males and females with low mercury concentrations.16

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We investigated maternal mercury concentrations and incubation behavior in a

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population of wild, free-living tree swallows. Using temperature dataloggers placed within

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nests, we compared several metrics of incubation behavior including incubation constancy

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(proportion of each day the female spent incubating eggs), the number of incubation recesses

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taken per day, and incubation recess duration to two indices of mercury exposure: a female’s


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blood mercury concentration and the mercury concentration of her eggs. We predicted that

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females with higher mercury concentrations would exhibit lower incubation constancy, take

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longer and more frequent incubation recesses, and their eggs would be more likely to experience

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substantial decreases in temperature. By conducting this study on a wild, free-living population,

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we examined incubation behavior over a range of naturally occurring mercury concentrations

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and in the presence of other natural environmental stressors.

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MATERIALS AND METHODS

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Study Area and Species

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We studied tree swallows nesting at the Cosumnes River Preserve (38.3ºN, 121.4ºW), an area

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comprised of more than 20,000 hectares of wetlands, uplands, and agricultural lands in

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California’s Central Valley. Historic mining activities within the Cosumnes River watershed,

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have led to extensive mercury contamination within the Cosumnes River, and wetlands within

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the preserve promote mercury methylation and bioaccumulation.36 In 2012, we installed 185

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artificial, wooden nest boxes, constructed using a design developed specifically for swallows

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(http://golondrinas.cornell.edu/). Nest boxes were set approximately 2 m above the ground and

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supported using 1.8-cm diameter metal conduit.

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Tree swallows are small, insectivorous songbirds that breed in a variety of habitats

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throughout North America.37 As a cavity-nesting species, tree swallows readily nest within

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artificial nest boxes, making them an attractive species for scientific research.

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Females typically lay between four and seven eggs in a clutch and incubate them for 13-14 days

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(range:11-20 days) before they hatch.37 Although at times males have been observed on the eggs

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during unusually cold weather, typically only the female incubates.37



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Measuring Nest Temperature

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Beginning in early April 2014, we visited nest boxes 1-2 times per week to document nesting

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activity. During nest visits, we counted the number of eggs in the nest and estimated the

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developmental age of the eggs by flotation.38,39 For nests found during egg laying, we estimated

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clutch completion date by counting forward, assuming one egg was laid per day, until the final

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clutch size was reached. For nests found after clutch completion, we estimated clutch

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completion date by subtracting the average developmental age of the eggs (estimated by

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flotation) from the date of the first visit. For nests found prior to, or 0-1 days after clutch

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completion, we placed an iButton temperature datalogger (Model DS1922L-F5#, Maxim

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Integrated Products, Inc. Sunnyvale, California, USA) into the center of the nest bowl amongst

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the eggs. To record ambient temperature within the nest box, we used double-sided tape to

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attach a second iButton datalogger to the interior of the nest box wall (that contained the

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entry/exit hole) at approximately the same height as the nest bowl datalogger. Prior to

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deployment, we programmed dataloggers to record temperature data at 2-min intervals, which

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allowed for 11 days of continuous data capture before the internal memory of the datalogger was

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filled. To limit disturbance and observer influence on nest attendance and incubation behavior,

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we only visited nests once a week (after the dataloggers were deployed) to remove dataloggers

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for data download and deploy new dataloggers. We continued weekly nest visits and datalogger

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replacement until the nest failed or the chicks fledged. If we found that the nest bowl datalogger

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had been moved from or buried in the nest between visits, we omitted the data for that nest

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during the preceding week.

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Using iButton Temperature Data to Evaluate Incubation Behavior

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Using SAS/STAT software (release 9.4, SAS Institute, Cary, North Carolina, USA), we adapted

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code from Croston et al.40 that uses an iterative process to identify incubation recesses and

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quantify incubation constancy for each nest from iButton temperature data. We considered nest

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temperature decreases that met certain criteria (described below) to be indicative of incubation

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recesses. Over the course of the study (16 April-26 June), nest bowl temperatures (mean±SD:

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34.4±3.3°C) were greater than ambient temperatures within nest boxes (19.7±7.6°C) 99% of the

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time (n=374,527 temperature data points; average temperature difference=14.7°C). Even during

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the hottest part of the day (12:00-18:00), nest bowl temperatures (35.4±3.5°C) were greater than

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ambient temperatures within nest boxes (27.1±6.1°C) 97% of the time (n=94,813 temperature

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data points; average temperature difference=8.3°C). Thus, in most instances, nest temperatures

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would be expected to decrease whenever an attending female departed from the nest for an

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incubation recess.

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For each nest, we identified all the time intervals where nest temperature decreased

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monotonically (i.e., temperature decreased over the interval and never increased during the

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interval). The end of these intervals consisted of any temperature increase, representing the

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female’s return to the nest and resumption of incubation. Next, we calculated the change in

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temperature from the beginning to the end of each monotonically decreasing interval and

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considered a temperature decrease of ≥1.5°C, occurring within the first 10 minutes of the

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interval, to be indicative of an incubation recess. Previous studies of tree swallows have used

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similar criteria and temperature decreases to identify incubation recesses.31,41 We then proofed

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the resulting dataset by creating time series temperature plots for each nest on each day and

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overlaying the identified incubation recess intervals (Figure S1). Once we had identified all the



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individual incubation recesses for each nest, we calculated three metrics of incubation behavior

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for each nest: (1) incubation constancy on each day, defined as the proportion of all temperature

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data points in which we interpreted the nest was being attended and the eggs were being

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incubated, (2) number of incubation recesses on each day, and (3) duration (in minutes) of each

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incubation recess.

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Although incubation constancy reveals how often incubating females are on and off the

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nest, it does not necessarily reflect the ultimate effect on egg temperatures or embryonic

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development. Therefore, we also determined if maternal mercury concentration affected the

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probability that the nest temperature would decrease by an amount likely to slow the rate of

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embryonic development. Optimal egg temperature for embryonic development is around 37°C

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and 26°C has been termed physiological zero temperature, below which embryonic development

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is suspended.42,43 However, our methods did not allow for the precise measurement of egg

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temperature. In fact, average incubation temperatures ranged from 32° to 37°C among nests,

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likely the result of subtle differences in the placement of the iButtons and the extent of iButton

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contact with the female’s brood patch. Because of these differences, we concluded that

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determining how often the temperature at the nest decreased below a fixed temperature value

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was not appropriate. Instead, for each identified incubation recess, we determined if the nest

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temperature decreased below 80% of the average incubation temperature for that specific nest.

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We chose a value of 80% because it represented approximately 5% of data with the most

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extreme decreases in incubation temperature observed. Thus, 80% of the average incubation

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temperature represented a substantial temperature drop that likely slowed the rate of embryonic

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development. Using this approach, the likelihood that an incubation recess resulted in a

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substantial temperature decrease would not be influenced by differences in measured nest


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temperatures due to differences in iButton placement in the nest or contact with the female’s

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brood patch.

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In order to validate our identification of incubation recesses, we compared incubation

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patterns inferred from iButton temperature data to field observations during which we recorded

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female presence and absence from the nest box. We observed 10 nests over approximately 7.5

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total daylight morning hours using a 20-60× spotting scope. Although this test is an imperfect

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comparison (a female inside a nest box may not necessarily be actively incubating), incubation

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status inferred from iButton temperature data agreed with field observations 90% of the time.

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Most apparent errors were caused by a delay in nest temperature to decrease following female

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departure from the nest box. This delay caused some very short recesses (

Mercury exposure and altered parental nesting behavior in a wild

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