Review Monitoring Forest Phenology in a Changing World Ross E. J. Gray * and Robert M. Ewers Department of Life Sciences, Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot, Berkshire SL5 7PY, UK; [email protected] * Correspondence: [email protected] Abstract: Plant phenology is strongly interlinked with ecosystem processes and biodiversity. Like many other aspects of ecosystem functioning, it is affected by habitat and climate change, with both global change drivers altering the timings and frequency of phenological events. As such, there has been an increased focus in recent years to monitor phenology in different biomes. A range of approaches for monitoring phenology have been developed to increase our understanding on its role in ecosystems, ranging from the use of satellites and drones to collection traps, each with their own merits and limitations. Here, we outline the trade-offs between methods (spatial resolution, temporal resolution, cost, data processing), and discuss how their use can be optimised in different environments and for different goals. We also emphasise emerging technologies that will be the focus of monitoring in the years to follow and the challenges of monitoring phenology that still need to be addressed. We conclude that there is a need to integrate studies that incorporate multiple monitoring methods, allowing the strengths of one to compensate for the weaknesses of another, with a view to developing robust methods for upscaling phenological observations from point locations to biome and global scales and reconciling data from varied sources and environments. Such developments are needed if we are to accurately quantify the impacts of a changing world on plant phenology. Keywords: drones; ecosystem change; methods; monitoring; phenology; remote sensing; UAVs Citation: Gray, R.E.J.; Ewers, R.M. Monitoring Forest Phenology in a Changing World. Forests 2021, 12, 297. 1. Introduction https://doi.org/10.3390/f12030297 Phenology is the study of the timing of recurrent biological events (or phenophases), the causes of these timings in regard to the biotic and abiotic drivers, and the connection Academic Editor: Luisa Frati among phases of the same or different species [1]. Here, phenology is defined by both describing observable events and also by describing the links and cascading indirect Received: 1 February 2021 effects that phenological events can have on an ecosystem [2]. This obvious interrelation Accepted: 2 March 2021 of phenology with so many aspects of an ecosystem is why it was hardly considered Published: 5 March 2021 a scientific discipline until the 1900s [3], despite the recording of phenological events dating back thousands of years [4] (Figure1). Nevertheless, the connection of phenology Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in with multiple facets of the ecosystem makes monitoring it critical for developing our published maps and institutional affil- understanding of ecological processes and for managing resources in the face of climate iations. and habitat change [5,6]. As such, there has been a rapid acceleration in the study of phenology and the associated development of new methods and technologies to aid this endeavour (Figure1). The past two decades in particular have seen increased effort to build interdisciplinary phenological research frameworks that utilise developments in technology to monitor phenology and its links with ecosystem function across species, Copyright: © 2021 by the authors. space and time [4,6,7]. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Forests 2021, 12, 297. https://doi.org/10.3390/f12030297 https://www.mdpi.com/journal/forests Forests 2021, 12, 297 2 of 24 Forests 2021, 12, x FOR PEER REVIEW 2 of 24 Figure 1. Timeline history of monitoring phenology. References for the specific time periods are: pre-1700 [4], 1700s [8], 1853Figure [9], 1900s 1. Timeline [10,11 ],history 1920s of [12 monitoring], 1950s [13 phenolo], 1960sgy. [14 ,References15], 1965-83 for [16 the–19 sp],ecific 1900s time [20 ],periods 2003 [ 21are:], 2000spre-1700 [3, 22[4],], 20071700s [ 23[8],,24 ], 1853 [9], 1900s [10,11], 1920s [12], 1950s [13], 1960s [14,15], 1965-83 [16–19], 1900s [20], 2003 [21], 2000s [3,22], 2007 [23,24], 2012 [2,25–27], 2016 [28,29], and 2020 [30]. 2012 [2,25–27], 2016 [28,29], and 2020 [30]. 1.1.1.1. The The Ubiquitous Ubiquitous ImportanceImportance of Plant Plant Phenology Phenology MostMost biologicalbiological organisms organisms foll followow certain certain life life cycle cycle events events,, but plant but plant phenology phenology is ar- is guably the most studied. Plant phenology includes processes such as leaf emergence, arguably the most studied. Plant phenology includes processes such as leaf emergence, flowering, fruiting, seeding and leaf senescence, and these processes link strongly to eco- flowering, fruiting, seeding and leaf senescence, and these processes link strongly to system function and services (Figure 2; [6,31]). Therefore, change to phenological events ecosystem function and services (Figure2;[ 6,31]). Therefore, change to phenological events may have implications for biogeochemical cycles, including that of carbon [32], and for may have implications for biogeochemical cycles, including that of carbon [32], and for the population dynamics of species connected at different trophic levels or in competitive the population dynamics of species connected at different trophic levels or in competitive and mutualistic interactions [33,34]. Plant phenology can further force temporal shifts in and mutualistic interactions [33,34]. Plant phenology can further force temporal shifts in animal phenology [22,35], with the potential for phenological mismatching if the species animalinvolved phenology do not respond [22,35], similarly with the to potential environmental for phenological changes [35,36]. mismatching if the species involvedLeaf do emergence not respond (flush) similarly phenology to environmental (the presence changesof new leaves [35,36 ].on a tree canopy) is particularlyLeaf emergence important, (flush) as it directly phenology controls (the processes presence such of new as primary leaves onproductivity, a tree canopy) car- is particularlybon sequestration, important, nutrient as it directlycycling, controls water storage, processes and such competition as primary and productivity, coexistence carbondy- sequestration,namics (Figure nutrient 2; [37–42]). cycling, For example, water storage, when canopy and competition trees flush and their coexistence leaves it alters dynamics the (Figurewater and2;[ 37light–42 environments]). For example, for coexisting when canopy organisms trees flushby intercepting their leaves more it altersof the theincom- water anding lightsolar environmentsradiation and reducing for coexisting throughfall organisms from precipitation, by intercepting increasing more ofsoil the water incoming up- solartake radiationand consequently and reducing reducing throughfall soil water from and precipitation, soil water evaporation increasing rates soil water (Figure uptake 2; and[38,43]). consequently Indirectly, reducing leaf flush soil can water alter and the soilpresence water of evaporation herbivorous rates insects (Figure and2 ;[conse-38,43]). Indirectly,quently shift leaf the flush presence can alter of the insectivorous presence of birds herbivorous and mammals insects (Figure and consequently 2). For instance, shift the presencephenological of insectivorous change of oil-seed birds and crops mammals has resulted (Figure in 2changes). For instance, in the abundance phenological and changetype ofof oil-seed herbivorous crops insects has resulted present in in changes agricultural in the landscapes, abundance inand turn type causing of herbivorous diet shifts in insects in- presentsectivorous in agricultural birds [44]. There landscapes, is also a infeedback turn causing loop to dietthis process: shifts in some insectivorous plant species birds aim [44 ]. Thereto reduce is also herbivory a feedback by loopaltering to thistheir process: phenolog someical plantactivity species to flush aim before to reduce insects herbivory emerge, by alteringor by synchronising their phenological their leaf activity flushing to flush with before other plant insects species emerge, to reduce or by synchronising herbivory pres- their leafsure flushing [31]. Tropical with otherplants plant that flush species their to leaves reduce later herbivory in the season pressure can suffer [31]. Tropicalsignificantly plants thathigher flush damage their leaves by insects later compared in the season to those can sufferthat flush significantly early or in higher synchrony damage during by insectsthe comparedpeak flushing to those phase that [45]. flush This earlyis not oralways in synchrony the case in during temperate the regions peak flushing however, phase where [45 ]. This is not always the case in temperate regions however, where variation in leaf flush timing involves ecological trade-offs. For example, some Oak species (Quercus spp.) in Eastern Europe flush early in the season to avoid summer droughts but consequently Forests 2021, 12, x FOR PEER REVIEW 3 of 24 Forests 2021, 12, 297 3 of 24 variation in leaf flush timing involves ecological trade-offs. For example, some Oak spe- cies (Quercus spp.) in Eastern