Introduction
Shifts in phenology, i.e., the timing of seasonal biological events, are
among the most noticeable impacts of human-caused global change
(Cleland et al., 2007;
Parmesan, 2007). Numerous studies have shown that recent climate
warming advances the timing of spring events, e.g., budburst, breeding
of amphibians, and arrival of migrating birds
(Parmesan, 2007; While
and Uller, 2014; Cohen et al., 2018). Beyond global climate change,
large-scale landscape modification can also impact phenology. For
example, urbanization has been shown to advance the timing of seasonal
events such as plant flowering, in part through the urban heat island
effect (reviewed in
Neil and Wu, 2006). However, more recent work has revealed that
urbanization can also delay phenological events, especially in warmer
regional climates (Li
et al., 2019), although the mechanisms driving these delays have yet to
be determined. Overall, there is considerable variation in phenological
responses to global change both within and among species
(Edwards and
Richardson, 2004; Thompson and Clark, 2006; Park et al., 2019). If
interdependent species differentially respond to human-mediated changes,
phenological mismatches may occur with potentially significant, negative
demographic consequences
(Miller-Rushing et
al., 2010; Renner and Zohner, 2018).
Better understanding insect phenological responses is critical given
their vast diversity, temperature-dependent developmental timing, and
critical role in ecosystems and the services they provide. These
services include dung burial, pest control, pollination, and wildlife
nutrition and are valued at over $57 billion annually in the United
States (Losey and
Vaughan, 2006). Further, several recent papers have reported dramatic
declines in insect populations
(Hallmann et al.,
2020; Wagner, 2020), potentially due to human-caused land-use change,
climate change, introduced species, and pollution
(Wagner et al.,
2021). Phenological shifts may
exacerbate losses due to mismatches, but might provide a means to adapt
to warmer temperatures and could even lead to overall population growth
rates, particularly in species that can successfully add a generation
due to extended growing seasons
(Kerr et al., 2020).
Most insect phenological studies focus on how climate drives theemergence of insects. In general, warmer-than-average years cause
adult insects to emerge earlier
(Bartomeus et al.,
2011; Roy et al., 2015; Villalobos-Jiménez and Hassall, 2017). Much
less is known about what determines termination or total duration of
insect activity
(Forrest, 2016).
Given extended growing seasons for many plant species
(Steltzer and Post,
2009), it might be expected that insects also delay termination of
adult insect activities in warmer regions. Longer growing seasons are
increasing the number of generations per year (voltinism) of some
insects (Altermatt,
2010a; Pöyry et al., 2011), but many species are obligate univoltine
across their entire range, including warm regions
(Forrest, 2016). For
these reasons, life history traits, known to be important in determining
insect activity
(Diamond et al., 2011;
Zografou et al., 2021), may strongly determine adult insect
termination. For example,
Stemkovski et al.
(2020) found that timing of bee emergence was most influenced by
climatic variation, but termination of adult bee foraging was better
explained by life history traits. Specifically, bee species that nest
below ground ended foraging earlier than species nesting above, but bee
species that overwinter as prepupae ended foraging later than those that
overwinter as pupae
(Stemkovski et al.,
2020).
Interannual regional climate variation is not the only driver of insect
phenology. Urbanization is in general leading to earlier flowering in
many plant species due to the urban heat island effect, although these
responses may be complex and context dependent
(Jochner and Menzel,
2015). Less is known about insects’ phenological response to
urbanization. The emergence of some insect species appears to be
advancing in urbanized areas
(Diamond et al., 2015;
Chick et al., 2019), but other studies have found no change in
phenology across urbanization gradients, despite phenological advances
in co-occurring plant species
(Seress et al., 2018;
Fisogni et al., 2020). The interaction between urbanization and
regional temperature can be an important driver of spatial phenology
patterns, as urbanization appears to advance plant phenology in cold
areas but causes delays in warm areas
(Li et al., 2019).
Diamond et al. (2014) also demonstrated that the urbanization effect on
phenological responses of butterflies depends on regional temperature.
This expected interaction between urbanization and temperature remains
untested at larger spatial scales and across a broader range of insect
groups.
Establishing generalities about determinants of emergence, termination,
and duration of adult insect activity is challenging because most
phenological research relies on surveys that provide much needed
information on species’ population abundance but are limited spatially
and taxonomically. Recent enormous growth in open and freely accessible
and curated community science photographs, such as those available via
the iNaturalist platform, are allowing researchers to ask novel
phenological questions at greater spatial and taxonomic scales
(Li et al., 2021).
However, careful data curation and specialized analytical methods must
be used to generate biologically meaningful results
(Larsen and Shirey,
2021).
Here we use community science generated digital vouchers and digitized
museum specimens to investigate how the emergence, termination, and
total duration of adult insects varies spatially in response to climate
and urbanization. We also examine
how such responses differ across species-specific life history traits.
We predict strong interactions between traits and key climate
predictors. For example, we expect the seasonal activity of insects with
thermally buffered larval stages to be less sensitive to variation in
temperature than species without thermally buffered larval stages,
aligning with a recent study on bees
(Stemkovski et al.,
2020). We further predict adult duration to vary based on voltinism,
with multivoltine species showing stronger responses to temperature than
univoltine species. Lastly, we predict adult insect termination to be
later and adult duration longer in warmer and urbanized areas,
consistent with recent studies in plants
(Li et al., 2021).