Autumn, the Neglected Season in Climate Change Research
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TREE-1899; No. of Pages 8 Review Autumn, the neglected season in climate change research 1 1 2 Amanda S. Gallinat , Richard B. Primack , and David L. Wagner 1 Department of Biology, Boston University, 5 Cummington Mall, Boston, MA 02215, USA 2 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 ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2015.01.004 warming climate. Trends in Ecology & Evolution xx (2015) 1–8 1 TREE-1899; No. of Pages 8 Review Trends in Ecology & Evolution xxx xxxx, Vol. xxx, No. x Table 1. Autumn has received less attention than spring in the Drivers of autumn phenology a 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