DOI: 10.5061/dryad.mcvdncjxh
title: Concordance of long-term shifts with climate warming varies among phenological events and herbaceous species

description: Many temperate herbs now flower earlier than a few decades ago. Little is
 known about other phenological events, despite the importance of life
 history integration for plant fitness. This study addresses the hypothesis
 that temporal shifts of multiple phenological events in herbs are
 concordant with temporal changes in weather. Explicitly showing that
 changes in timing of annual life cycle events are correlated with changes
 in weather-predicting variables provides support for the hypothesis that a
 phenological shift is concordant with climate change. Observations of six
 phenological events and five phenophases were made year-round for 25 yrs
 for herb species in a deciduous forest fragment, Trelease Woods in
 Illinois, USA. Dates for 43 species were analyzed by linear mixed-effects
 models for events and phenophases, and were compared to weather data from
 a nearby station. For early species, Emergence was delayed by 1.5
 d/decade, while End Expansion advanced by 3.8 d/decade and Begin Dormancy
 advanced by 2.5 d/decade. For late species, End Expansion advanced by 6.7
 d/decade, while Begin Senescence delayed by 17.7 d/decade. Begin Flowering
 and End Flowering advanced similarly for both seasonal groups, at 3.8 to
 4.2 d/decade. Some events showed no temporal change. Species differed
 greatly in the degree or direction of change, related to seasonality of
 event or length of phase. Overall, for a given species, most events are
 advancing (68.4%) and most durations are shortening (74.4%). In 12 of 13
 cases, inter-annual variation in event date was predicted by a temperature
 event-season combination variable, but in only six cases did both event
 date shift and weather variable warm through time. This finding supports
 the hypothesis that climate change is associated in changes in some, but
 not all, phenological events. This first long-term, multi-phase study of a
 community of temperate herb species indicates little temporal coherence of
 responses of multiple phases. Changes in date are event-specific,
 phase-specific, and species-specific. This complexity of responses among
 species and uneven responses within a species’ integrated annual cycle
 events has implications for evolutionary responses and more immediate
 interactions among plant, animal, and microbe species in this community.
description: DATA SET 1: 1993-2017
 Observations of annual phenological
 events for 50 herbaceous species were made in Trelease Woods, a 24.5 ha
 fragment of temperate deciduous forest, dominated by canopy trees of sugar
 maple near Urbana, IL, USA.  Elevation varies by &lt; 5m.  The 25
 1-m<sup>2</sup> quadrats observed were <i>≥</i> 50
 m from the edge in a 50 m x 50 m grid in the north half of the
 Woods.  The phenological status of each
 species in each quadrat was determined by the same observer (CKA) weekly
 in spring and summer, biweekly in fall, and biweekly to monthly in winter
 from 1993 – 2017.  For each species in each quadrat, dates of six
 phenological events were used to calculate five durations of phenophases. 
 Thus, measurements were recorded, and later analyzed, at the quadrat
 level.  Quadrats differed in number and size of individuals; regardless,
 the first (or last) individual in the quadrat to begin or end a phase
 defined the event date for that species in that quadrat Species were analyzed together in
 seasonal groups (Appendix S2: Table S1).  It was not logistically
 practical to build climate models for 43 species separately for up to six
 events and five durations.  For most events, species were grouped as early
 or late (Table 1, Appendix S2: Table S1).            
 We used linear mixed-effects models to test for phenological changes
 through time, and the weather variables that had the most predictive power
 of phenological events.  To address temporal trends in phenology, we
 tested 13 total phenological response variables in separate analyses for
 the dates of six events and 11 for the durations of five phases. 
 Individual quadrat observations, in each year, were used in the analyses. 
 For each phenological variable, we used model selection to find the top
 model at the seasonal group-level with respect to fixed effects and random
 effects structure.  All models included random effects terms for the
 species and quadrat, and the two were treated as crossed random effects. 
 Therefore, the analysis also provided species-specific temporal
 changes.            For analyses of the relationship
 between phenological events and weather variables (Appendix SI: Text S3),
 we tested the dates of six phenological events in 13 separate analyses
 based on seasonal groups of species.  Fixed effects consisted of weather
 variables, and in some cases phenological variables that preceded the
 response, the “legacy” effects.  Weather variables described temperature
 and precipitation in individual months or seasons, and differed for each
 group of response variables (Appendix S2: Table S3).  The random effect of
 species was included in all models.              We
 completed three main steps to select weather variables that were most
 predictive of an event (see Appendix S1: Text S3 for details): 1) For each
 weather variable, individually determine the random and fixed effects
 structures for the top model predicting the phenological event.  Eliminate
 from further consideration those weather variables that were not included
 as a fixed effect. 2) Among correlated weather variables, choose the
 strongest predictor.  Exclude weather variables not in the top model
 predicting the phenological event.  Eliminate from further consideration
 those weather variables not included as a fixed effect, i.e. that are
 correlated with a stronger predictor.  3) Test different combinations of
 the remaining fixed effects, highlighting the top models and the weather
 variables they include.             DATA SET 2:
 1949-1964             Observations of the
 same six events of eight of the same species (genus in case of
 <i>Viola</i> spp.) were made at unknown frequency from
 1949-1964 by Charles Smith, woods custodian.  The location from 1949-1956
 was noted as Brownfield Woods (5 yrs) or Trelease Woods (6 yrs) or both in
 the same year (3 yrs); no location was given for 1957-64.  Prior to
 19<sup>th</sup> century deforestation, the two woods were in
 the Big Grove.  Today, the distance between the two fragments is &lt;2
 km.  Descriptions by Smith are: first appearance above ground (= Emergence
 by CKA), leaves full grown (= End Expansion), begin flowers (= Begin
 Flowering), end flowers (= End Flowering), leaves begin to color (=
 Senescence), leaves all fallen/withered (= Dormancy).  Differences between
 means for each of 44 species-events were determined by t-tests.
description: DATA SET
 1: 1993-2017 A cell mumber
 for each of the six phenological events is the Julian calendar date in one
 year of the first (or last) individual of a species in one of 25 1 m x 1 m
 quadrats exhibiting the event.  Negative numbers for Emergence and End
 Expansion refer to number of days prior to Julian calendar date 1.  A cell
 number for each of the five phenological durations is the number of days
 derived from subtraction of dates of two events (e.g. Expansion -
 Emergence = Expansion Duration).   Only
 non-italicized numbers were used in analyses (see Appendix S2: SI Table 5
 for summary of species and phenological events used in analyses).  Species
 varied from 1 - 25 quadrats and 6 - 25 years of observation.  Primary
 criteria for a species to be analyzed were &gt;15 years distributed
 relatively evenly over the 25 years; a minimum or constancy in number of
 quadrats were not required.  Italicized
 numbers were not used in analyses, either because of too few years and/or
 additional criteria based on a species’ natural history, including complex
 phenologies such as multiple leafing periods, and ability to apply
 consistent criteria of an event (Appendix S1: Text S1), e.g. if an
 inter-annual pattern in plant size was obvious, the species was not
 analyzed.   Missing data
 arose because a species appeared irregularly from year to year in a
 quadrat, an event did not occur in a quadrat in a given year (e.g.
 flowering, obvious senesence), or an event was not observed (particularly
 true of senescence/dormancy in autumn/winter or emergence of winter
 annuals in autumn).  The dominant reason for missing data or italicized
 data is provided under species name in the second column (see Appendix S1:
 Text 1 for details).  Also included are species nomenclature (following
 USDA, NRCS. 2019), family, and phenological syndrome, as well as
 miscellaneous notes of atypical phenology.   DATA SET 2:
 1949-1964 For 1949-1964,
 no methods are available, only data sheets.  A number is the Julian
 calendar date for a species in one of six phenological events in a given
 year; see Appendix S1: Text 1 for description of each event.  One date per
 species per year was recorded for each event; no variation was noted. 
 That date was assumed to represent mean values of a given event.  For
 comparison, mean values for each event for each year for each of the same
 eight species for 1993-2017 were calculated.