Discussion
For butterflies in Massachusetts, changes in abundance were most strongly associated with changes in flight period. Species that have extended their flight period have increased in abundance relative to those that have not. Past studies that have evaluated the effect of warming temperatures have generally demonstrated that species advancing phenological events under warming environmental conditions are generally increasing in abundance or have positive demographic growth (Cleland et al., 2014; Hulme, 2011; Ozgul et al. 2010; Willis et al., 2008; Møller et al., 2008). Species which fail to change their phenology, however, appear to be declining (MacGregor et al. 2019; Cleland et al., 2014; Willis et al., 2008; Møller et al., 2008). In many ways, our results parallel a recent study of Lepidoptera in the Britain (MacGregor et al., 2019). In both studies, changes in some phenological metric were associated with increases in abundance, especially in multivoltine species. However, in contrast to Britain, trends in the mean timing of activity of Massachusetts butterflies were not strongly associated with trends in abundance. Instead, changes in the flight period were the best predictor of trends in abundance. In Massachusetts, changes in flight period were driven more by extended late-season activity than advanced onset of activity, which also contrasts with past work in Britain (Roy and Sparks, 2000). Our results highlight the importance of evaluating the entire temporal distribution of a phenological phenomenon, as opposed to simply using trends in mean observation dates.
One possible mechanistic explanation for the association between extended flight period and increased abundance is an increase in the number of generations per year. In other insect species, climate warming may allow for faster larval development and the production of additional direct-developing generations before adverse winter conditions (MacGregor et al., 2019; Miton & Ferrenberg, 2012; Altermatt, 2009; Tobin et al., 2008). Visual inspection of representative species in our data suggest that at least some populations are adding, at least, a partial generation (Fig. 1b, c & e). For example, Satyrdotes appalachia (Appalachian Brown, Fig. 1b) may be transitioning from univoltine to bivoltine in our region (Stichter, 2015). If additional generations are the causal mechanism between changes in flight period and increased abundance in multivoltine species, it would suggest that beneficial effects of higher population growth rates (Kerr et al., 2020) and/or more rapid evolution (Chevin et al., 2010) outweigh the potential costs of developmental traps (Van Dyck et al., 2015; Levy et al., 2015). In general, multivoltine butterfly species seem to have higher population growth rates than univoltine species in north-temperate climates (MacGregor et al., 2019; Wepprich et al., 2019; Breed et al., 2013). In one study from a Mediterranean climate, however, multivoltine species showed significantly steeper declines than obligate uni- or bivoltine species. In this ecosystem, seasonal adversity in summer months via drought may have led to a developmental trap (Melero et al., 2016).
Past studies of butterflies in Massachusetts (Breed et al., 2013) and of other Lepidoptera (Pöyry, 2009; Parmesan et al., 1999) have revealed strong patterns of poleward range shifting in response to climate change. In Massachusetts, southern species are increasing in relative abundance, and northern species tend to be declining (Breed et al. 2013). Our structural equation model suggests one causal pathway by which southern species are increasing in relative abundance to some extent because of their capacity to extend their overall flight period. Although the SEM supports variability in voltinism as the strongest driver of trends in abundance, there were also direct effects of species’ range type on trends in abundance. These effects presumably reflect other limiting factors such as physiological tolerance or trends in interacting species. For example, Nymphalis vaualbum (Compton Tortoiseshell, Fig. 1a) is a northern species that has recently declined rapidly in the state of Massachusetts. The abrupt shift in abundance suggests a physiological threshold could have been crossed in the past decade.
For at least two species in our data, changes in flight period appeared to be due in part to changes in the ability to overwinter in Massachusetts, as opposed to voltinism per sePoanes zabulon Zabulon skipper (Fig. 1b) and Battus philenor Pipevine swallowtail (Fig. 1c) were formerly considered vagrants. In other words, in the past, individuals of these species moved annually to Massachusetts from populations further south during the summer, but never established resident populations (Stichter, 2015). It seems likely that these species can now successfully overwinter in Massachusetts, as shown by an apparent early season generation (see Fig. 1b & c). These trends contrast with two other migratory species, Vanessa cardui (Painted Lady, Fig. 1d) and Danaus plexippus (Monarch, Fig. 1f), both which are non-resident, multi-generational, obligatory migrants, far north of overwintering sites. Both species have delays (not advances) in the onset of spring activity in Massachusetts, and only V. cardui showed delayed end of flight activity, while there was no substantial trend in the end of D. plexippus flight in Massachusetts. Both species showed negligible changes in relative abundance in Massachusetts.
Across the community of butterflies in Massachusetts, trends in abundance estimated from counts, as well as trends from the list length analysis, were centered on zero. In other words, approximately equal numbers of Massachusetts species are increasing in abundance as are declining in abundance. Our results contrast with negative average trends reported across butterfly communities in four other regions: Ohio, USA (Wepprich et al. 2019), California, USA (Forister et al. 2011), the UK (Brereton et al. 2018), and Spain (Melero et al. 2016). Unlike Ohio and California, both of which have agricultural development at industrial scales, Massachusetts may be subject to lower levels of agricultural land use intensification. Systematic monitoring rather than ad hoc citizen science observations would be needed to rigorously test whether butterfly communities in Massachusetts are truly more stable in abundance when compared to other regions. Nonetheless, our data suggest a hopeful hypothesis that butterflies may be able to adjust to climate change, if freed from the additional pressure of anthropogenic changes in land use.
Our results highlight the potential for phenological changes to affect population dynamics, and the general importance of phenological flexibility for insect population dynamics in changing environments. Past studies of phenology have rarely evaluated shifts in the end of activity (Zipf al., 2017; Gallinat et al., 2015), despite the demographic importance of late-season events such as entry into diapause (Kerr et al. 2020). Unlike traditional metrics of phenological change, quantile regression (Cade & Noon, 2003) enabled us to estimate trends in both the onset and end of flight across Massachusetts butterflies. In Massachusetts, changes in the total flight period and end of activity were associated more strongly with trends in abundance than onset or mean trends. In Lepidoptera, a diversity of cues and mechanisms, both genetic and plastic (Lindestad et al., 2019; Kozak et al., 2019), shape patterns of phenology and voltinism. Understanding these mechanisms would be a valuable direction for future research if our goal is to predict changes in phenology and abundance in new systems. This case study highlights how phenological changes relate to population dynamics, and the importance of phenological changes for population viability in changing environments.