Autumn, the Neglected Season in Climate Change Research

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Review

Autumn, the neglected season in climate change research

1 1 2

Amanda S. Gallinat , Richard B. Primack , and David L. Wagner

Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02215, USA

Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, U-43 Storrs, CT 06269, USA

Autumn remains a relatively neglected season in climate identify ﬁve areas ripe for future research, and provide

change research in temperate and arctic ecosystems. recommendations for research in those areas.

This neglect occurs despite the importance of autumn

events, including leaf senescence, fruit ripening, bird and What we know about autumn

insect migration, and induction of hibernation and dia- In temperate ecosystems, the autumn phenomena that have

pause. Changes in autumn phenology alter the repro- received the most attention in climate change research are

ductive capacity of individuals, exacerbate invasions, leaf senescence and migratory bird departures. Insect

allow pathogen ampliﬁcation and higher disease-trans- diapause and fruit ripening have also garnered moderate

mission rates, reshufﬂe natural enemy–prey dynamics, interest. Other autumn phenomena such as amphibian

shift the ecological dynamics among interacting species, dormancy and bud formation remain less studied and poorly

and affect the net productivity of ecosystems. We syn- understood.

thesize some of our existing understanding of autumn Despite the relative neglect of autumn, ecologists have

phenology and identify ﬁve areas ripe for future climate made important progress in understanding the drivers of

change research. We provide recommendations to ad- autumn phenology and the effects of climate change on

dress common pitfalls in autumnal research as well as to autumn events (Figure 1). Long-term observational data-

support the conservation and management of vulnera- sets indicate that leaf senescence is, on average, delayed by

ble ecosystems and taxa. increasing temperatures [4,5]. In addition, community-

and landscape-level studies show that invasive non-native

The neglect of autumn plants can gain an advantage over native species by

Numerous effects of climate change on the spring phenol- extending their growing seasons in autumn [6], and that

ogy (see Glossary) of temperate plants and animals are an extended growing season allows many perennials to

well documented [1,2]. Warmer temperatures have sequester more carbon – which in turn alters local climate

resulted in earlier leaf-out and ﬂowering of plants, earlier and ecosystems [7]. Long-term data indicate that birds are

arrivals of migratory songbirds, and earlier emergence and shifting their autumn phenology in response to climate

spring migration of insects [3,4]. Autumn, by contrast, has change, with short-distance migrants generally delaying

received less attention: in the publication database Scopus migration and some long-distance migrants leaving earlier

there are only about one-half to one-third as many climate [8–10]. Insects that have been examined have responded to

change studies set in autumn as compared to spring

(Table 1). The neglect of autumn in phenology and climate

change research is likely caused by a combination of fac- Glossary

tors, including the complexity of drivers of autumn phe-

Autumn migration: the annual long-distance movement of individuals from

nology, the protracted nature of autumn events, and

their breeding ground to their wintering ground. In the northern hemisphere,

human enchantment with the sudden burst of spring autumn migrants typically fly north to south. Many temperate- and arctic-

breeding birds migrate in autumn, as do insects such as monarch butterflies

ﬂowers and wildlife following winter.

and some dragonflies.

Despite this relative neglect, autumn events are also

Diapause: a physiological state of dormancy. In arctic and temperate

hugely important ecologically and evolutionarily. They ecosystems, diapause is a hormonally driven hiatus in developmental or

reproductive processes. Diapause can occur in any life-stage, and is an

signal the end of the growing and breeding season for most

important overwintering strategy for insects and other animals.

temperate and arctic plant and animal species, and are an

Leaf senescence: leaf aging, resulting in a decline in function, that in temperate

understudied component of the ecological impacts of regions is associated with seasonal leaf-color change and leaf drop. Plants

reabsorb essential nutrients from their leaves before autumn leaf senescence.

climate change. In the following review we synthesize some

Net ecosystem productivity (NEP): for an ecosystem, the balance between

of our existing understanding of autumn phenology,

carbon sequestered through photosynthesis and the carbon lost through

respiration. Warming autumn temperatures can delay leaf senescence and

extend photosynthesis and the growing season, but can also disproportio-

nately increase ecosystem respiration.

Corresponding author: Gallinat, A.S. ([email protected]). Phenology: the timing of seasonal biological events. Spring events including

Keywords: phenology; climate change; fruit; diapause; leaf senescence; migration. flowering, leaf-out, and insect emergence have been shown to advance in

response to warming temperatures. Autumn events such as leaf senescence

0169-5347/

and autumn migration are less well studied, but are often delayed by a

warming climate.

Trends in Ecology & Evolution xx (2015) 1–8 1

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Table 1. Autumn has received less attention than spring in the Drivers of autumn phenology

climate change literature While various measurements of spring temperature can

‘Climate Change’ ‘Autumn’ ‘Spring’ Autumn (%) explain most of the variation in leaﬁng-out times [14], au-

Climate Change (CC) 3248 8751 27.1 tumn senescence is more weakly linked to autumn tempera-

‘Leaf*’ and ‘CC’ 212 549 27.9 tures [15] (Figure 2), as well as to the combination of

‘Bird*’ and ‘CC’ 100 413 19.5

temperature and photoperiod [7,16]. Other less-predictable

‘Insect*’ and ‘CC’ 73 188 28.0

factors can explain additional variation; for example, drought

‘Fruit*’ and ‘CC’ 63 À

can advance leaf coloring and leaf drop while abundant soil

15.4

moisture can delay senescence [17]. Early frost events and

‘Flower*’ and ‘CC’ À 346

high winds can also result in sudden leaf senescence and

‘Mammal*’ and ‘CC’ 39 108 26.5

abscission [18,19]. Air pollution in the form of tropospheric

‘Amphibian*’ and ‘CC’ 7 32 17.9

a ozone can induce early senescence, while local CO2 con-

Results from a Scopus search conducted on December 11, 2014. The ﬁrst search

centration has been reported to have no effect [18,20].

included ‘climate change’ (CC) and either ‘autumn’ or ‘spring’ (the terms ‘fall’,

‘autumnal’, and ‘autumn*’ yielded many false hits, whereas the terms ‘spring’ and Insect diapause and migration phenology also vary

‘autumn’ yielded a large fraction of relevant titles and abstracts). Each subsequent

substantially among species and are often modeled as a

search included ‘climate change’, as well as either ‘autumn’ or ‘spring’ and a

combination of photoperiod and temperature [21]. Al-

taxon/plant organ search term, as listed in the left-hand column of the table (the

asterisk represents the truncation/wildcard term). Results include the number of though most temperate insect species appear to rely in

publications returned for all years. Autumn (%) indicates the percentage of the

part on photoperiod controls to induce diapause, some

total citations for each taxon that include autumn in title, keywords, or abstract.

The percentage for fruit is based on the combined fruit and ﬂower total. species such as the parasitoid wasp Leptopilina japonica

and the European corn borer (Ostrinia nubilalis) enter

warmer autumn temperatures with faster developmental diapause in response to minimum temperatures or daily

rates, added generations, and delayed migration and temperature cycles alone [22,23]. For autumn-migrating

diapause [11,12]. Fruit ripening of native plants, by con- insects, migration timing is also usually driven by day

trast, is the only autumn event of which we are aware to length and temperature, but it can also be affected by

have advanced, on average, in response to warming tem- rainfall, humidity, host plant senescence, and wind [12,24].

peratures [4,13]. As we will describe, changes in autumn The timing of autumn bird migration is driven by many

phenology can also increase the reproductive capacity of factors, and species-speciﬁc interactions among factors,

individuals, exacerbate invasions, alter the ecological dy- including environmental conditions (e.g., temperature

namics among interacting species, and affect the net pro- and photoperiod), life-history traits (e.g., broodedness

ductivity of ecosystems. and wintering location), spring arrival times, migration

Advancing Delaying Refs

Single-brooded species Mulple-brooded species Long-distance migrants Short-distance migrants [8–10] Bird departures

Mulvolne species Univolne species Temperature-driven diapause [12,43,66] Insect diapause

A few late ﬂowering species Fruit Most species Increasing presence of invasives [13,30,67] ripening

In drought condions Most species, wet years Leaf [4,7,68]

senescence

Aug Sept Oct Nov Dec

TRENDS in Ecology & Evolution

Figure 1. Expected phenological shifts of autumn events in response to climate change. We indicate how leaf senescence, bird departures, fruit ripening, and insect diapause

are expected to respond to climate change in temperate ecosystems of eastern North America. Gray broken lines indicate the direction in which an event will shift; darker

stippling indicates a response that is common, while lighter stippling indicates a response that is comparatively rare. Some of these changes are happening already. The data for

leaf senescence and bird migration are most complete, while there is far less information on fruit maturation times and insect diapause. [4,7–10,12,13,30,43,66–68]

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0.9 Key: Leaf out 0.8 Leaf senescence 0.7 ) 2 0.6 0.5 0.4 0.3

by temperature (R 0.2

Variaon in date explained Variaon 0.1 0 Betula Aesculus Fagus Quercus pendula hippocastanum sylvaca robur Species

TRENDS in Ecology & Evolution

Figure 2. Temperature explains more variation in spring than in autumn leaf phenology. Correlation coefficients (R ) between event date and the preceding mean monthly

spring and autumn temperatures for four tree species in Germany (1951–2000). Data from [15].

speed, and endogenous circannual rhythms. The propor- It is clear from the recent autumn literature that

tional inﬂuence of these drivers varies widely among researchers will have to deviate from spring methodology

species, migratory cohorts, and geographies [8–10,25,26], to appropriately capture autumn events. Autumn deﬁni-

and requires further, widespread investigation using tions must be biologically relevant and comparable across

multivariate analyses. studies, and this could require treating autumn phenome-

na as multiple-day events [31].

Methods for studying autumn phenology

Compared to those that take place in the spring, observa- The inﬂuence of autumn on carbon storage

tional studies of autumn phenology are faced with greater Autumn phenology plays an important role in the annual

methodological challenges, such as deﬁning events, stan- carbon balance of temperate ecosystems. Later senescence

dardizing methodologies, and treating autumn phenomena dates contribute to longer growing seasons in temperate

as multiple-day events. It is apparent that many autumn and arctic regions [32]. Wu et al. [33] found that changes in

studies, for example those of leaf senescence and fruit autumn leaf phenology in temperate forests better explain

maturation, are based on somewhat subjective observa- variation in annual net ecosystem productivity (NEP) – in

tions such as ‘50% leaf fall’ or descriptions of fruit colors other words, the balance between photosynthesis and

[4,27]. In addition, most researchers do not adequately respiration – than do changes in spring phenology. Delayed

describe their methods, making it difﬁcult to compare autumn leaf senescence is associated with increased NEP,

records across studies. meaning that ecosystems tend to sequester more carbon in

One challenge for deﬁning autumn events is that warmer years with later autumn phenology [7,34,35]. How-

although spring events such as leaf-out and insect emer- ever, this result is not universal; autumn warming also

gence are sudden and visually apparent, autumn events elevates ecosystem respiration, occasionally outweighing

such as leaf senescence, fruit ripening, and bird and increased autumn production, which can turn current

butterﬂy migration are protracted and asynchronous. carbon sinks into future CO2 sources [36].

Deﬁnitions of leaf-out in spring are similar, and occur The variety of factors affecting autumn NEP complicates

within days of one another; by contrast, deﬁnitions for attempts to forecast the implications of longer growing

the date of senescence range from the date of ﬁrst leaves seasons on NEP. At the Harvard Forest in Massachusetts,

changing color to the date of 100% abscission — events spring ecosystem respiration is dominated by respiring

that can occur weeks apart [28,29]. Autumn bird migra- foliage, but autumn respiration is dominated by below-

tion is also temporally extended, and can involve multi- ground root and microbial respiration [37]. Furthermore,

ple waves of migrating birds [3]. Fruits typically mature although they are often lumped together as ‘soil respiration’,

over an extended period as well, as part of their repro- root and microbial respiration differ in their responses to

ductive and dispersal strategy, which contrasts with the environmental change [38]. The phenology of roots and

sudden and brief ﬂowering-window for many species microbial activity is poorly understood, and observations

[30]. Thus, it is not possible to assign single dates to suggest substantial variability in root phenology of temper-

many autumn phenomena. It is also more difﬁcult to ate tree species [39]. In addition, root phenology cannot be

observe the last date of activity for a species in the determined from above-ground plant phenology [40]. The

autumn than the date of its ﬁrst appearance in spring lack of data regarding the partitioning of above-ground, root,

because absence can be more challenging to observe than and soil microbial phenological responses to climate change

presence, and, in the case of birds, autumn behavior is remains a large limitation in our understanding of, and

less conspicuous [3]. ability to forecast, how autumn climate change will

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inﬂuence carbon sequestration. Given the magnitude and have the potential to infect people with Lyme disease

importance of above- and below-ground arctic and temper- [46]. Delayed onset of winter allows ampliﬁcation of both

ate carbon resources, the need for more ecosystem-level mosquito populations and their viruses [47]: human infec-

studies and models addressing autumnal phenomena tions of West Nile virus are much more prevalent in the

remains great. fall, and some mosquito vectors are known to take a larger

fraction of their blood meals from mammals in the fall

Invasive species, pests, and pathogens in autumn following the departure of migratory birds [48]. Similarly,

Phenotypic plasticity and rapid evolution allow some inva- wildlife such as caribou (Rangifer tarandus) are expected

sive species to be more responsive to warmer autumn to experience a longer infective season by the nematode

temperatures and later freezing events than are many Ostertagia gruehneri with warmer temperatures in the

native species [41]. Fridley [6] found that many non-native spring and autumn, thus increasing their likelihood of

invasive shrub species in the eastern USA gained an infection [49] (Figure 4).

advantage of greater autumn carbon assimilation over Much published literature focuses on invasive species,

native shrub species through delayed leaf senescence in pests, and pathogens that stand to beneﬁt from climate

autumn, rather than via earlier leaf-out in the spring change. Certainly, there will also be disadvantaged inva-

(Figure 3). Thus, the lengthening growing season likely sive species, pests, and pathogens. For instance, while

contributes to the advantage some invasive species, such some insect pests experience faster development times

as Morrow’s honeysuckle (Lonicera morrowii) and Glossy and increased generations, others respond to increased

buckthorn (Rhamnus frangula), have over many native temperatures (those beyond their optimum range) with

shrubs, and might be considered as a bet-hedging strategy slower development times, lowered reproductive capacity,

to maintain viable leaves despite the increasing risk of and increased mortality [50]. Many sap-feeding insects

frost damage. respond to water-stressed host plants and decreased hu-

Warmer autumn temperatures also present an advan- midity with shorter lifespans, lowered fecundity, and ele-

tage for some insect pests. By speeding development and vated dispersal rates [51,52]. We also expect within-species

delaying diapause, many insects produce more generations regional variation in the effects of climate change on

in warmer, longer growing seasons [42]. The diapause of autumn insect abundance based on temperature thresh-

Spruce beetles (Dendroctonus ruﬁpennis) and Douglas ﬁr olds and range shifts. For instance, although native ash

beetles (Dendroctonus pseudotsugae), for instance, can be trees (Fraxinus sp.) in the northern USA are expected to

either disrupted or delayed with warmer autumn tempera- experience heightened herbivory from the introduced em-

tures, extending both reproductive capacity and feeding erald ash borer (Agrilus planipennis), trees that occur at

activity [43]. Already, warmer autumn and winter weather lower latitudes are predicted to experience decreased her-

has allowed bark beetle populations to increase and has bivory from the beetle [53].

magniﬁed damage to trees in the western USA and Canada.

There are consequences for human health as well. Interspecies interactions

Warmer autumns have led to extended autumn activity Species rely on synchrony for interspeciﬁc interactions in

of ticks and mosquitoes [44,45]. Ticks (e.g., Ixodes species) autumn, exactly as they do in spring and other seasons.

continue to search for blood meals in autumn as long as Some insects lay their eggs on particular fruits, birds

temperatures remain above their activity thresholds, and consume particular types of fruit during migration, and

0.10 * 0.08 0.06 *

*** 0.04 Non-nave > nave 0.02 0.00

Lonicera Viburnum Rhamnaceae ElaeagnaceaeCelastraceae Other naves Lonicera korolkowii Lonicera Lonicera fragranssima Lonicera Euonymus bungeanus Euonymus Lonicera japonica Lonicera Lonicera sempervirensLonicera Elaeagnus mulflora Diervilla lonicera Lonicera periclymenum Lonicera Viburnum lantana Diervilla rivularis Frangula alnus Frangula Lonicera morrowii Lonicera Berberis vulgaris Lonicera maackii Lonicera Euonymus europaeus Euonymus Elaeagnus angusfolia Lonicera standishii Lonicera Elaeagnus umbellata Viburnum sieboldii Viburnum edule americanum Zanthoxylum Berberis koreana Lonicera xylosteum Lonicera Celastrus scandens Celastrus Ptelea trifoliata Ptelea Viburnum segerum Calycanthus floridus Calycanthus Dirca palustris Dirca Viburnum opulus Lonicera x bella Lonicera Sambucus racemosa Berberis thunbergii Viburnum dilatatum Euonymus phellomanus Euonymus Frangula caroliniana Frangula Sambucus nigra Lonicera tatarica Lonicera Lonicera canadensis Lonicera Cornus amomum Lonicera ruprechana Lonicera alatus Euonymus Viburnum nudum Viburnum prunifolium Rhamnus catharca Viburnum dentatum Viburnum lentago Hydrangea arborescens americanus Euonymus Viburnum acerifolium Celastrus orbiculatus Celastrus Hamamelis virginiana Cornus florida Shepherdia argentea Euonymus hamiltonianus Euonymus Lonicera reculata Lonicera albus Symphoricarpos Elaeagnus commutata Viburnum rafinesqueanum villosa Lonicera Lindera benzoin Cornus alternifolia Acer pensylvanicum Acer Euonymus obovatus Euonymus atropurpureus Euonymus Rhamnus alnifolia spicatum Acer Viburnum lantanoides Rhamnus davurica oblongifolia Lonicera involucrata Lonicera acuminata Clethra * * * * * * * * * Proporon C gain in autumn C gain Proporon 0.0 0.1 0.2 0.3 0.4 Plant species in rank order

TRENDS in Ecology & Evolution

Figure 3. Non-native invasive plants gain an advantage over native species with extended autumnal growth. Mean proportions (with standard errors) of seasonal carbon (C)

assimilation (of total carbon assimilation) by native (green) and non-native (red) species (many of which are invasive) in autumn (after approximately 24 October). Many

non-native species are better able to assimilate carbon in the autumn, and extend their growing season in comparison with native species. Colored asterisks on the bottom

right reflect autumn carbon gain of less than 0.5%. The inset depicts comparisons between native and non-native members of different phylogenetic groups, with asterisks

denoting the significance of comparisons (*, P<0.05; ***, P<0.001). Reproduced from [6].

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0.06 their hosts have been conducted in the spring when emer-

gence asynchrony can be dramatic. The more subtle appear-

/C)

ance of autumn phenomena does not mean that they have

0.04 smaller effects on population dynamics – rather it means

that much further study in this area is warranted.

Even within a taxon the consequences of climate change

0.02 are complex and are likely to have both positive and

negative effects. Taking the Monarch butterﬂy as an

example, several studies have warned that climate change

threatens the overwintering roosts in Mexico [60], and

Temperature-dependent 0

reproducve success (R

0 100 200 300 there is mounting evidence that droughts in the south-

central and southwestern USA have contributed to the

Julian date

butterﬂy’s recent demographic collapse across eastern

TRENDS in Ecology & Evolution

North America [61]. However, warmer average tempera-

Figure 4. A warming climate will extend the infective period of the nematode tures and prolonged autumnal conditions are favorable to

(Ostertagia gruehneri), which causes disease in the caribou (Rangifer tarandus). In

larval development, and will shift the milkweed range to

four seasonal climate scenarios, with black, blue, green, and red representing

make more plants available to Monarchs in Canada and

successively warmer climates, the temperature-dependent reproductive success of

the nematode (indicated by the index Ro/C) is predicted by a model to start earlier the northern USA [62].

in the year and extend later in the year as conditions warm. Nematode

reproductive success, and its resulting ability to infect hosts, declines in summer

The future of autumn research

as a result of the decreased ability of the nematode to survive hot weather.

Reproduced from [49]. Based on what is already known about autumn events, and

the conspicuous gaps in our overall understanding on the

topic, we make ﬁve core recommendations for future

many specialist insect folivores feed into autumn research into the effects of climate change on autumn

[12,30,54]. Asynchrony can result when interacting species phenology.

experience different magnitudes or directions of phenologi- (i) Researchers should use factorial experiments and

cal shift in response to climate change. In spring, climate large-scale, multispecies observational studies to deter-

change has resulted in asynchrony between herbivores and mine the mechanisms affecting autumn events, as well as

leaves, ﬂowers, and pollinators, and between migratory the underlying phylogenetic signals. Information on the

birds and their insect prey, in some cases leading to factors controlling autumn events currently comes almost

decreases in survival and reproductive success [55– entirely from small-scale observational studies. Experi-

57]. The variability of temporal shifts in autumn also creates ments that test the effects and interactions of factors –

possibilities for asynchrony, but these remain little studied. such as temperature, soil moisture, frost events, host-

Songbirds primarily consume fruits during autumn plant quality, and photoperiod – will make it possible to

migration, and many plants rely on birds to disperse their isolate and quantify the drivers of leaf senescence, fruit

seeds [30]. However, climate change is advancing fruit- ripening, and insect diapause. Similarly, large-scale, mul-

ripening dates and delaying songbird departures for many tispecies studies will help to quantify the role of shared

species [4,10]. This mismatch will change songbird diets, evolutionary history of closely related species in inﬂuenc-

particularly for those short-distance migrants that depart ing fall phenology. The ﬁndings that experimental warm-

late in the season. Invasive non-native plants often pro- ing studies underpredict the inﬂuence of temperature on

duce abundant fruits of low nutritional quality that last spring phenology, and that phenology is often phylogenet-

later into the autumn season [30,58]. Because many song- ically conserved, reinforce the importance of isolating

birds delay departures as a consequence of a warming drivers experimentally, accounting for phylogeny, and of

climate, they will likely feed more on the fruits of invasive comparing experimental ﬁndings to long-term observa-

species, increasing invasive seed dispersal. tional studies [1,63–65].

The possibility of mismatches involving insects is both (ii) Autumn events should be methodologically and

intriguing and largely unknown. Because invertebrates statistically treated as multiple-day events rather than

often have short generation times and large brood sizes, single dates, and deﬁnitions should be standardized where

most have great capacity for tracking climate changes. possible. We encourage researchers to treat autumn events

Monophagous insects that feed on developing seeds and as multiple-day events, recording the beginning, duration,

fruit might experience changing food resources if climate and end of autumn phenomena, and analyzing changes in

change affects their developmental timing. Additional each of these three response variables [31]. This approach

broods will extend the presence of some species, exposing avoids the challenge of developing robust single-day deﬁni-

them to new complexes of predators, parasitoids, and patho- tions for each autumn event, and more accurately reﬂects

gens. The tachinid ﬂy Compsilura concinnata, introduced ecological reality. Where possible, researchers should aim to

into North America from Europe to control gypsy moth [59], record metrics – such as chlorophyll content or coloration –

is now successfully producing an additional fall generation on a continuous scale, making it possible to then determine

in New England (Jeff Boettner, personal communication), rates of senescence, points of inﬂection in the season, or the

which parasitizes late-season notodontid moth caterpillars timing of markers such as 50% change [7].

and other non-target species. Almost all the studies Future research should prioritize the development and

documenting asynchrony between parasitoid insects and standardization of common empirical techniques and

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deﬁnitions, such as those developed by the USA National many long-distance migrant bird and insect species al-

Phenology Network [31], for the sake of spatial and tem- ready in decline due to loss of breeding, wintering, and

poral comparisons. Leaf senescence observations could be stopover habitat, as well as other threats, mismatches for

standardized through the use of handheld chlorophyll long-distance migrants should receive special attention.

meters and leaf litter measurements, and fruit-ripening These mismatches are not limited to the complete loss of

dates could be standardized with reference color samples interactions – instead they can alter the quality of inter-

and sugar content measured with a refractometer. Emerg- actions, such as effects on the abundance or nutritional

ing technologies should be applied to standardizing quality of food, or on the strength of competitive or mutu-

autumn phenology measurements: smartphone apps for alistic interactions [55,56]. Adaptive plasticity will serve to

citizen scientists can enhance the spatial resolution of mitigate some phenological mismatch through individual

phenological observations, while geolocator tags and adjustments. However, mismatches will likely still take

GPS tracking devices can be used to monitor the depar- effect at the community scale. Future studies should aim to

tures of inconspicuous migratory birds with improved explore these relatively subtle effects of phenological

accuracy and detail. changes on the quality of food and other factors, particu-

(iii) Further research should examine the separate larly for specialized and otherwise vulnerable groups, such

effects of climate change on the phenologies of above- as long-distance bird and insect migrants, organisms with

ground, root, and microbial respiration, and assess the complex cycles, and species with small effective population

effects of changes in autumn phenology on the cycling of sizes. Thus, research in these areas will inform manage-

carbon and other key nutrients. Models that account for ment recommendations that can help to protect key inter-

the differential changes in above-ground, root, and micro- actions for rare and otherwise imperiled species.

bial respiration are necessary for reasonable forecasts of While we have focused here on ﬁve important research

the effects of climate change on NEP and the cycling of areas, there are other gaps in our knowledge of how climate

carbon and nutrients. These components will be most change impacts on autumnal phenomena. Remarkably few

easily differentiated by experiments examining the effects studies have followed the carry-over impacts of autumnal

of warmer, drier autumns on the magnitude and phenology conditions on the following spring or followed individuals

of root and microbe respiration below ground, as well as across multiple years. Another exciting topic in much need

above-ground respiration of leaves and wood. The domi- of study is the extent to which autumn responses to climate

nance of autumn below-ground respiration in carbon losses change are genetic versus plastic. Do autumnal responses

makes separating root and microbial respiration, and have more plasticity built into them than their vernal

measuring widely across the temperate landscape, impor- counterparts? We have the sense that organisms do more

tant next steps for reducing error in carbon cycling models. bet-hedging in the fall, perhaps because the ﬁtness con-

The Keenan et al. [35] method of combining satellite data, sequences for encountering frost are lower in autumn than

biosphere models, and ecosystem-level carbon ﬂux mea- in the spring – and, if so, what are the underlying mecha-

surements with long-term ﬁeld observations is an excellent nisms that allow such plasticity in response?

example of synthesizing approaches to investigate the

effects of climate change on NEP. Expanding such meth-

Conclusions

odologies will allow better worldwide projections of carbon

Research has identiﬁed many of the primary environmen-

balance and feedbacks to climate change in autumn.

tal drivers of autumn phenology. However, much uncer-

(iv) Researchers should investigate the role of autumn

tainty remains about the relative contributions of different

climate change on the success of pests, pathogens, and

drivers, how they interact with species’ life-histories, and

invasive species, and the importance of these ﬁndings for

how temporal shifts will manifest at the community and

recommended management practices. Given the dispro-

ecosystem level. What we have outlined here are promising

portionate inﬂuence of pests, pathogens, and invasive

avenues for future research in autumn phenology, and

species on ecosystems and society, forecasts of the effects

possible implications for conservation management. This

of climate change and phenological changes must take

ﬁeld remains wide open for discovery, particularly by way

these factors into account [49]. Moreover, given the success

of experiments, mechanistic modeling, and observations of

of particular invasive plant species and pests in the au-

species interactions. We urge ecologists to study the effects

tumn, conservation agencies might need to adjust how they

of climate change and phenological changes in the autumn

identify which species are of the highest priority to man-

window – as very many studies have already accomplished

age. For effective management of these groups and their

for the spring.

ecological communities, researchers should identify the

features (e.g., origin site, feeding strategy, minimum tem-

Acknowledgments

perature optimum) common to invasive species, pests, and

We thank Abe Miller-Rushing, Pamela Templer, John Silander, Ernest

pathogens that beneﬁt from autumn climate change, as

Williams, Elizabeth Ellwood, Rose Abramoff, Yingying Xie, Katie Todd,

well as how changes to these groups impact upon species in

Karen Oberhauser, Margaret Boeni, and Caitlin McDonough MacKenzie

the surrounding community. for their helpful comments and suggestions, and Caroyln Mills for

(v) Finally, autumn phenology changes have the poten- assistance with the literature searches. We also thank Ally Phillimore

and an anonymous reviewer for detailed and thoughtful reviews. This

tial to result in ecological mismatches and dietary changes

work was supported in part by a National Science Foundation Graduate

among interacting species; priority should be given to

Research Fellowship under Grant DGE-1247312 (to A.S.G.), a Humboldt

studying species, such as specialists and migrants, that

Research Award (to R.B.P.), and United States Department of Agricul-

are particularly vulnerable to environmental change. With ture (USDA) grant COOP #14-CA-11420004-138 (to D.L.W.).

TREE-1899; No. of Pages 8

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