Evaluating Phenological Mismatch Between Bird Migration and Insect Emergence:

The Warbling Vireo and Eastern Tent Caterpillar

By Marcella Willett

Introduction:
Climate change has caused shifts in the phenologies of many organisms. According to
one meta-analysis from 2003, spring events across many species were shifting earlier by an
average of 2.3 days per decade (Parmesan & Yohe, 2003). Another meta-analysis from 2003
found an average shift of 5.1 days earlier per decade (Root et al., 2003). However, these shifts
are not consistent across different organisms, causing the phenologies of interacting organisms
to shift relative to each other (Kharouba et al., 2018; Visser & Gienapp, 2019). This can cause a
phenological mismatch, such as when the abundance of a resource does not align with the
timing of the consumer’s demand (Visser & Gienapp, 2019). A 2018 study found that 57% of
interacting species had phenologies shifting closer together, while 43% had phenologies shifting
further apart (Kharouba et al., 2018).
This paper focusses on evaluating whether climate change is altering the phenological
synchrony of bird migrations relative to insect emergence. Many studies have found that birds
have been arriving at their breeding grounds earlier with increases in temperature (Gienapp et
al., 2007; Hurlbert & Liang, 2012; Koleček et al. 2020). However, birds that migrate longer
distances do not adjust their migrations based on temperature as much as birds with shorter
migrations (Koleček et al., 2020). Insects also generally emerge earlier in warmer years (Forrest,
2016). This effect is strongest for insects that are active early in the season, which in addition to
emerging earlier, have also generally been staying active later in warmer years (Forrest, 2016).
However, not all insect species follow this pattern (Forrest, 2016).
In order to investigate the interaction between birds and their insect prey, this study
focusses specifically on the warbling vireo (Vireo gilvus) and the Lepidoptera caterpillars they
prey on. A vireo species was chosen because, for the purposes of this analysis, it was simpler to
focus on a bird that preys heavily on a certain type of insect. According to an analysis of
photographs of birds carrying insects, 64% of the insects that vireos caught to feed to their
young were in the order Lepidoptera (Kennedy, 2019). This was one of the highest percentages
of one insect order in the diet of a specific bird family (Kennedy, 2019). The warbling vireo
specifically was chosen because it is widespread across much of the US during its breeding
season and is known to feed on caterpillars (Cornell Lab of Ornithology, n.d.).
I hypothesize that both warbling vireo spring migration and Lepidoptera caterpillar
emergence will shift earlier, but potentially to different extents which could create a
phenological mismatch.

Methods:
I collected data on insect emergence from the USA National Phenology Network (USA-
NPN). The species of Lepidoptera caterpillars I initially chose for analysis were the bicolored
sallow moth (Sunira bicolorago), Canadian tiger swallowtail (Papilio canadensis), eastern tent
caterpillar (Malacosoma americanum), giant swallowtail (Papilio cresphontes), pipevine
swallowtail (Battus philenor), spongy moth (Lymantria dispar), western tent caterpillar moth
(Malacosoma californicum), and woolly bear (Pyrrharctia isabella). These species were chosen
because these were the caterpillars available on USA-NPN that belong to the families that
vireos prefer to eat: Noctuidae, Erebidae, Notodontidae, Lasiocampidae, and Papilionidae
(Kennedy, 2019). I left the date range on the USA-NPN Phenology Observation Portal (from
which the data was downloaded) open to from 1950-01-01 to 2021-12-31 to encompass all
possible complete years of data. The phenophase category was limited to “Development” to
focus specifically on the caterpillar phase of those species. I downloaded data separately from 8
states that had the largest numbers of records (MA, ME, MI, MN, NY, PA, TN).
The two types of caterpillars which had consistent data across several years in a state
were the eastern tent caterpillar and the woolly bear caterpillar. However, in most of the states
with woolly bears (MI, PA, NY), they were documented sporadically throughout the year
without a clear start and end of season, so they would not have worked well for my analysis.
Therefore, I only used eastern tent caterpillars for this study. Furthermore, I had to limit the
states for analysis to Massachusetts and Tennessee because the other states did not have data
from enough years for eastern tent caterpillars.
I downloaded individual phenometrics data to analyze the earliest sightings of
caterpillars at each site in each state, in addition to magnitude phenometrics data to find the
peak of caterpillar sightings each year and better determine the start and end of the caterpillar
season. When analyzing the individual phenometrics data I pulled out the earliest sightings of
either phenophase “caterpillars” or phenophase “caterpillars feeding” at each site. I did not
include “caterpillars in tent” because it would likely be difficult for the birds to catch a
caterpillar in a tent. To analyze the magnitude phenometrics data, I focused specifically on the
phenophase “caterpillars.” I recorded the start of caterpillar season, which I defined as the
starting day of year (DOY) of the first week with a “yes” record, as well as the end of caterpillar
season, the starting DOY of the last week with “yes” records. I did not include the start or end if
there was not a week with 0 “yes” records before (for the start) or after (for the end) because
this would imply that no one had checked the site in the weeks around the week with “yes”
records and the caterpillars could have been out during those week. I also recorded the peak of
caterpillar season, which I defined as the starting DOY of the first week with the highest
proportion of “yes” records to total records.
After analyzing the caterpillar data, I turned to the data on the warbling vireo. I used bar
chart data from the Cornell Lab of Ornithology’s eBird database. eBird is a citizen science
network where birders record the number and species of birds they see. I used the “frequency
data” which is how often the bird was recorded on completed checklists because it would likely
provide an accurate proxy for how many birds were in the state. I recorded the start and end of
the vireos in the state, which I defined as the DOY of the first day of the first and last week
respectively where the frequency was 0.01 or greater. I also recorded the peak, the DOY of the
first day of the first week with the highest frequency.
Results:

Fig.1. Start, peak, and end of warbling vireo frequencies in 3 states

The start and peak of warbling vireo frequencies remained relatively constant over time
in both states (Fig.1) However, there was more variation in the end dates. In Tennessee, the
end DOYs ranged between 265 and 289, and slope of trendline showed that the end dates
increased by around 1.964 days per year (Fig.1.b). In Massachusetts, the end dates were more
constant; the DOYs ranged between 274 and 319, and according to the trendline, the end date
only increased by 0.536 days each year (Fig.1.a).

Fig.2. Top: Individual Phenometrics data on eastern tent caterpillars in 2 states. The red outlying data points are
not included in the calculations of the trendlines. Bottom: Start, end and peak of eastern tent caterpillar season
collected from Magnitude Phenometrics data in 2 states.
 The trends for the eastern tent caterpillars varied by states and the measurement used.
In Massachusetts, the individual phenometrics data showed a slight increase in the DOY the
caterpillars were first sighted, with a trendline slope of 0.393 (Fig.2.a). However, the magnitude
phenometrics data showed a decrease in the DOYs of the start, peak, and end, with trendline
slopes of -5.022, -6.103, and -4.627, respectively (Fig.2.c). In Tennessee, the individual
phenometrics data showed also showed a slight increase, with a trendline slope of 0.643 after
the omission of an outlying late data point at one site in 2015 (Fig.2.b). The magnitude
phenometrics data showed a slightly steeper increase in the start and end, with trendline
slopes of 3.174 and 2.679 respectively, but a shallower increase in peak, with a trendline slope
of 0.25 (Fig.2.d). The magnitude data is likely a better indicator of whether the timing of
caterpillar availability is shifting because it includes three different parts of the caterpillar
season and does not include first “yes” records that were not preceded by a “no” record soon
before.

Fig.3. The start, peak, and end of eastern tent caterpillar and warbling vireo graphs overlayed with pink
shading between the start and end trendlines for warbling vireos and blue shading between the start and
end trendlines for eastern tent caterpillars.

By overlaying the data and trendlines from the vireos and caterpillars, we can see if a
phenological mismatch is likely to occur (Fig.3) In Massachusetts, such a mismatch appears
likely to occur in the near future (Fig.3.a). The eastern tent caterpillar start, peak, and end dates
are getting earlier, while the warbling vireo start date remains constant. According to the
trendlines, the start and peak of the caterpillar season have already begun to move out of the
range of the vireo season. The slope of the end of caterpillar season trendline indicates that it
will likely also move out of the vireo season in the future, meaning that the entirety of the
eastern tent caterpillar season could occur outside of the warbling vireo season. The trendlines
in Tennessee indicate that caterpillar season is not likely to move out of vireo season (Fig.3.b).
Instead, the start and end dates of caterpillar season have been getting later and moving
further into vireo season. However, this could shift the caterpillar season such that the peak of
vireo season would no longer fall within the eastern tent caterpillar season.
Discussion:
My hypothesis was partially supported by the results of this study. Over the time period
measured in the study, warbling vireo earliest arrival date and peak remained constant, rather
than becoming earlier as my hypothesis suggested. Eastern tent caterpillar emergence trended
earlier in Massachusetts but trended later in Tennessee. In general, this study did find evidence
of potential phenological mismatch occurring in the future with the eastern tent caterpillar
season trending out of warbling vireo season in Massachusetts, and the caterpillar season
trending away from the peak of vireo season in Tennessee.
A major limitation of this study is the small amount of data used and the short time
frame of the data. The severely limited data, especially for caterpillars, could cause the trends
observed to be a result of the small sample size rather than reflecting the actual population.
Another limitation is that there is not enough data available on a wider variety of caterpillar
species, so this study had to focus only on the eastern tent caterpillar, which likely only makes
up a small part of the warbling vireo’s diet. A more comprehensive dataset of caterpillar
phenologies could greatly improve future research in this area. Additionally, the short time
span of the data used for this study prevents the observed trends from being ascribed
specifically to long-term climate changes. A future study could compare the dates for bird
migration and caterpillar activity to the temperature of each year or of each spring rather than
the chronological order of the years to assess whether the trends are being caused by climate
change.
The shorter-term time span of the data could account for why the warbling vireo arrival
date remained constant. Many studies have determined that bird arrival dates tend to shift
earlier in years with warmer temperatures (Gienapp et al., 2007; Hurlbert & Liang, 2012;
Koleček et al. 2020). This phenomenon has been documented in the red-eyed vireo (Hurlbert &
Liang, 2012), a close relative of the warbling vireo, so it may be likely to occur in the warbling
vireo as well. However, my analysis focused only on 2015-2021, which did not exhibit consistent
warming in spring temperatures in the US over the course of that time span (NOAA, 2022a).
Since arrival date correlates more closely with temperature than with chronological year
(Gienapp et al., 2007), this could explain why my study did not find any trends of warbling
vireos arriving earlier.
The differing results on the eastern tent caterpillar season in Massachusetts compared
to Tennessee can potentially be explained by looking at the average spring temperatures in
those states over the years measured. In Massachusetts, the caterpillar start, peak, and end
tended to shift earlier over the course of the study period (2015-2021), and the trendline of
average spring temperatures (March-May) increased over those years (NOAA, 2022b). In
Tennessee, the caterpillar start and end shifted later, and the trendline of average spring
temperatures was decreasing over the study period (NOAA, 2022b). This pattern fits with the
results of a 2005 paper analyzing the timing of peak caterpillar biomass in the Netherlands,
which found that peak biomass timing correlated closely with the temperature between March
8th to May 17th (Visser et al., 2005).
Because of the limited time frame, data, and caterpillar species analyzed this study does
not provide conclusive evidence as to whether warbling vireos are or will be experiencing a
phenological mismatch with their food supplies. However, if such a mismatch were
documented it could negatively impact vireo reproduction and population size. An unshifting
arrival date or an arrival date that is not shifting fast enough to keep up with the changing
phonologies of food supplies could limit the birds’ ability to shift their egg-laying date, as
documented in pied flycatchers (Both & Visser, 2001). When breeding date is not synchronized
with the availability of food, this can cause decreases in the number of fledged chicks and their
weight, which has been shown in great tits (Visser et al., 2005). Mismatch between breeding
dates and food availability has been shown to correlate with population declines in pied
flycatchers (Both et al., 2006). Future research in warbling vireos could look at whether their
egg-laying dates have been shifting in response to climate change and how that compares to
changes in the timing of caterpillar abundance.

Citations:
Both, C., & Visser, M. E. (2001). Adjustment to climate change is constrained by arrival date in a
long-distance migrant bird. Nature, 411(6835), 296-8.
https://doi.org/10.1038/35077063

Both, C., Bouwhuis, S., Lessells, C. et al. (2006). Climate change and population declines in a
long-distance migratory bird. Nature 441, 81–83. https://doi-
org.proxy122.nclive.org/10.1038/nature04539

Cornell Lab of Ornithology. (n.d.). Warbling Vireo. In All About Birds. Retrieved November 29,
2022, from https://www.allaboutbirds.org/guide/Warbling_Vireo/overview

eBird. (2021). eBird: An online database of bird distribution and abundance [web application].
eBird, Cornell Lab of Ornithology, Ithaca, New York. Available: http://www.ebird.org.
Accessed: November 25, 2021.

Forrest, J. (2016). Complex responses of insect phenology to climate change. Current Opinion
in Insect Science, 17, 59-54. https://doi.org/10.1016/j.cois.2016.07.002

Gienapp P., Leimu R., Merilä J. (2007). Responses to climate change in avian migration
time—microevolution versus phenotypic plasticity. Clim Res 35, 25-35.
https://doi.org/10.3354/cr00712

Hurlbert A. H., Liang Z. (2012) Spatiotemporal Variation in Avian Migration Phenology: Citizen
Science Reveals Effects of Climate Change. PLoS ONE 7(2): e31662.
https://doi.org/10.1371/journal.pone.0031662

Kennedy, A. C. (2019). Examining Breeding Bird Diets to Improve Avian Conservation Efforts
(Order No. 22618921) [Doctoral Dissertation, University of Delaware] University of
Delaware ProQuest Dissertations Publishing. http://nclive.org/cgi-
bin/nclsm?url=http://search.proquest.com/dissertations-theses/examining-breeding-
bird-diets-improve-avian/docview/2308261156/se-2
Kharouba, H. M., Ehrlén, J., Gelman, A., Bolmgren, K., Allen, J. M., Travers, S. E., & Wolkovich,
E. M. (2018). Global shifts in the phenological synchrony of species interactions over
recent decades. Proceedings of the National Academy of Sciences of the United States of
America, 115(20), 5211–5216. https://www.jstor.org/stable/26509509

Koleček, J., Adamík, P., & Reif J. (2020). Shifts in migration phenology under climate
change: temperature vs. abundance effects in birds. Climatic Change, 159(2), 177-194.
https://doi.org/10.1007/s10584-020-02668-8

NOAA National Centers for Environmental information, (2022a). Climate at a Glance: National
Time Series, retrieved on November 30, 2022 from
https://www.ncei.noaa.gov/access/monitoring/climate-at-a-glance/national/time-
series

NOAA National Centers for Environmental information, (2022b). Climate at a Glance: Statewide
Time Series, retrieved on November 30, 2022 from
https://www.ncei.noaa.gov/access/monitoring/climate-at-a-glance/statewide/time-
series

Parmesan, C. & Yohe G. (2003). A globally coherent fingerprint of climate change impacts
across natural systems. Nature, 421, 37-42. https://doi.org/10.1038/nature01286

Root, T. L., Price, J. T., Hall, K. R., Schneider, S. H., Rosenzweig, C., Pounds, J.A. (2003)
Fingerprints of global warming on wild animals and plants. Nature 421, 57–60.
https://doi.org/10.1038/nature01333

Visser, M. E., Holleman, L. J. M., & Gienapp, P. (2006). Shifts in Caterpillar Biomass Phenology
Due to Climate Change and Its Impact on the Breeding Biology of an Insectivorous Bird.
Oecologia, 147(1), 164–172. http://www.jstor.org/stable/20445808

Visser, M. E., & Gienapp, P. (2019). Evolutionary and demographic consequences of

phenological mismatches. Nature Ecology & Evolution, 3(6), 879-885.
https://doi.org/10.1038/s41559-019-0880-8

USA National Phenology Network. 2022. Plant and Animal Phenology Data. Data type:
Individual Phenometrics and Magnitude Phenometrics. 01/01/1950 - 12/31/2021 for
Region: MA, ME, MI, MN, NY, PA, TN. USA-NPN, Tucson, Arizona, USA. Data set accessed
11/21/2022 at http://doi.org/10.5066/F78S4N1V