ArticlePDF Available

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years

May 2023
American Journal of Botany 110(7)

DOI:10.1002/ajb2.16188

License
CC BY 4.0

Authors:

Matthew Austin

Missouri Botanical Garden

Show all 5 authorsHide

Premise: Although changes in plant phenology are largely attributed to changes in climate, the roles of other factors, such as genetic constraints, competition, and self-compatibility, are underexplored. Methods: We compiled >900 herbarium records spanning 117 years for all 8 nominal species of the winter-annual genus Leavenworthia (Brassicaceae). We used linear regression to determine the rate of phenological change across years and phenological sensitivity to climate. Using a variance partitioning analysis, we assessed the relative influence of climatic and non-climatic factors (self-compatibility, range overlap, latitude, and year) on Leavenworthia reproductive phenology. Key results: Flowering advanced by ~2.0 days and fruiting ~1.3 days per decade. For every 1°C increase in spring temperature, flowering advanced ~2.3 days and fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced ~6-7 days. The best models explained 35.4% of flowering variance and 33.9% of fruiting. Spring precipitation accounted for 51.3% of explained variance in flowering date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%, respectively. Year accounted for 16.6% of flowering variance and 5.4% of fruiting, and latitude 2.3% and 15.1%, respectively. Non-climatic variables combined accounted for <11% of the variance across phenophases. Conclusions: Spring precipitation, alongside other climate and climatically-related factors, were dominant predictors of phenological variance. Our results emphasize the strong effect of precipitation on phenology, especially in moisture-limited habitats preferred by Leavenworthia. Amongst the many factors that determine phenology, climate is the dominant influence, indicating the effects of climate change on phenology are expected to increase. This article is protected by copyright. All rights reserved.

Change in reproductive season climate over 117 years.

…

Variance partitioned in Leavenworthia (a) flowering and (b) fruiting dates.

…

Figures/Table S1-5).

…

Figures - uploaded by Adam B Smith

Content may be subject to copyright.

Content uploaded by Adam B Smith

Content may be subject to copyright.

Content uploaded by Adam B Smith

Content may be subject to copyright.

Received: 10 October 2022

Accepted: 29 May 2023

DOI: 10.1002/ajb2.16188

RESEARCH ARTICLE

Beyond the usual climate? Factors determining ﬂowering

and fruiting phenology across a genus over 117 years

Kelsey B. Bartlett

|Matthew W. Austin

|James B. Beck

|Amy E. Zanne

Adam B. Smith

Department of Geography, George Washington

University, Washington, D.C., USA

Living Earth Collaborative, Washington

University, St. Louis, MO, USA

Department of Biological Sciences, Wichita State

University, Wichita, KS, USA

Department of Biology, University of Miami,

Coral Gables, FL, USA

Center for Conservation and Sustainable

Development, Missouri Botanical Garden,

St. Louis, MO, USA

Correspondence

Kelsey B. Bartlett, 2036 H St. NW, Department

of Geography, George Washington University,

Washington, D.C. 20052 USA.

Email: bartlett.kelseyb@gmail.com

Abstract

Premise: Although changes in plant phenology are largely attributed to changes

in climate, the roles of other factors such as genetic constraints, competition, and

self‐compatibility are underexplored.

Methods: We compiled >900 herbarium records spanning 117 years for all

eight nominal species of the winter‐annual genus Leavenworthia (Brassicaceae). We

used linear regression to determine the rate of phenological change across years and

phenological sensitivity to climate. Using a variance partitioning analysis, we assessed

the relative inﬂuence of climatic and nonclimatic factors (self‐compatibility, range

overlap, latitude, and year) on Leavenworthia reproductive phenology.

Results: Flowering advanced by ~2.0 days and fruiting by ~1.3 days per decade.

For every 1°C increase in spring temperature, ﬂowering advanced ~2.3 days and

fruiting ~3.3 days. For every 100 mm decrease in spring precipitation, each advanced

~6–7 days. The best models explained 35.4% of ﬂowering variance and 33.9% of

fruiting. Spring precipitation accounted for 51.3% of explained variance in ﬂowering

date and 44.6% in fruiting. Mean spring temperature accounted for 10.6% and 19.3%,

respectively. Year accounted for 16.6% of ﬂowering variance and 5.4% of fruiting, and

latitude for 2.3% and 15.1%, respectively. Nonclimatic variables combined accounted

for <11% of the variance across phenophases.

Conclusions: Spring precipitation and other climate‐related factors were dominant

predictors of phenological variance. Our results emphasize the strong eﬀect of

precipitation on phenology, especially in the moisture‐limited habitats preferred by

Leavenworthia. Among the many factors that determine phenology, climate is the

dominant inﬂuence, indicating that the eﬀects of climate change on phenology are

expected to increase.

KEYWORDS

Brassicaceae, gladecress, global change, Leavenworthia, phenological shift, precipitation, relative humidity,

temperature, variance partitioning, winter annual

Earlier plant reproduction has been well documented in

response to climate change (Menzel et al., 2006;

Parmesan, 2006; Miller‐Rushing and Primack, 2008;

Ganjurjav et al., 2020), with some species advancing

phenology by up to 2.5 days per °C over 30 years (Menzel

et al., 2006). Climate cues contribute signiﬁcantly toward

phenological variance. For example, the accumulation of

days above or below certain temperature thresholds has a

strong eﬀect on the timing of germination, leaf‐out,

ﬂowering, and fruiting (Pemadasa and Lovell, 1974; Müller

and Schmitt, 2018; Meng et al., 2021). While advanced

phenology due to warming is the most commonly

Am J Bot. 2023;e16188. wileyonlinelibrary.com/journal/AJB

1of14

https://doi.org/10.1002/ajb2.16188

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the

original work is properly cited.

Amy E. Zanne and Adam B. Smith co‐last authors whose labs contributed equally.

documented response (Menzel et al., 2006; Miller‐Rushing

and Primack, 2008; Suonan et al., 2017; Piao et al., 2019),

other studies found contradictory outcomes, including

delayed phenology due to an unmet chilling requirement

(Yu et al., 2010; Hart et al., 2014) and advanced phenology

following regional cooling (Banaszak et al., 2020). Changes

in precipitation also interact with shifting temperature to

inﬂuence phenology in varied ways (Ganjurjav et al., 2020;

Zettlemoyer et al., 2021; Currier and Sala, 2022),

especially in moisture‐limited environments (Lesica and

Kittelson, 2010; Shen et al., 2015). Factors such as latitude

and year of observation are highly correlated with climatic

variation and are statistically associated with plant phenol-

ogy (Munguía‐Rosas et al., 2011; Yue et al., 2015). Focusing

solely on the eﬀect of climate, however, ignores the possible

inﬂuence of other variables. For example, the timing of leaf‐

out in the Northern Alps of Europe is best predicted when

latitudinal variation in photoperiod is incorporated along-

side temperature (Meng et al., 2021).

While climate change is a well‐known driver of

phenological shifts, we do not yet understand the relative

inﬂuence of climatic and non‐climatic factors on variance in

reproductive phenology. Phenological variation among

species is well documented (Harrison et al., 2015; Cole

and Sheldon, 2017), and this variation may reﬂect both

climatic and species‐, population‐, and community‐level

factors. For example, the degree of relatedness among

species can shape their reproductive timing (e.g., Raﬀerty

and Nabity, 2017; Mazer et al., 2021). Closely related species

may ﬂower at similar times due to genetic constraints

(Brearley et al., 2007; Davis et al., 2015) or ecological and

environmental factors (Gavini et al., 2021). On the other

hand, related, co‐occurring taxa may avoid coﬂowering

to better access pollinators and avoid heterospeciﬁc

pollen transfer (e.g., Campbell, 1985a,b; Stone et al., 1998).

Finally, diﬀering reproductive traits may also drive

phenological variation (Gorman et al., 2020). For example,

self‐incompatibility can aﬀect reproductive timing because

the ﬂowering time of individuals that rely on outcrossing

is constrained by the phenology of conspeciﬁcs and their

pollinators (Bartomeus et al., 2011).

Understanding phenological responses to diﬀerent

environmental factors requires long‐term data on the

timing of plant reproductive events. Herbarium (Davis

et al., 2015; Willis et al., 2017; Meineke et al., 2018; Austin

et al., 2022) and citizen science records (Belitz et al., 2020;

Iwanycki Ahlstrand et al., 2022) can provide a valuable

source of such long‐term data. Many herbaria contain

records spanning decades, if not centuries, with each record

preserving a specimen's unique phenological phase at a

certain time and place. Citizen science records are typically

more recent but are the fastest growing in biodiversity

databases (Barve et al., 2020). Such herbarium and citizen

science records can also contain further information

relevant to phenological studies, such as the year, species,

or coordinates of the collection.

In this study, we used herbarium and citizen science

records to examine the relative contribution of climatic

and nonclimatic factors on shifts in phenology across

the entire taxonomic and spatial distribution of a single

genus. Leavenworthia (Brassicaceae), commonly known as

gladecress, is a genus of herbaceous annuals (Rollins, 1963;

Al‐Shehbaz and Beck, 2010) found across the southern and

southeastern United States (Figure 1). While previous

studies have explored the causes and consequences of the

unique mating systems of Leavenworthia (Solbrig and

Rollins, 1977; Busch et al., 2010; Busch and Werner, 2012),

less attention has been paid to the factors shaping the

reproductive phenology within the genus (Banaszak

et al., 2020). Given that four of the eight species in the

genus are imperiled or critically imperiled (NatureServe

ranks G1 or G2; NatureServe, 2022) and one is listed under

the U.S. Endangered Species Act (U.S. Fish and Wildlife

Service, 2020), understanding this taxon's reproductive

timing is key to its conservation. Changing phenology

aﬀects the biotic and abiotic conditions under which plants

FIGURE 1 Leavenworthia occurrence records mapped by species. Each point corresponds to the centroid of the county of collection. Darker and/or

layered points indicate numerous records collected from a single county. Note the highly restricted range of most species in contrast to the broader

distribution of L. uniﬂora, the only species to span the Mississippi River.

2of14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

15372197, 0, Downloaded from https://bsapubs.onlinelibrary.wiley.com/doi/10.1002/ajb2.16188 by Cochrane Japan, Wiley Online Library on [02/07/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

reproduce, aﬀecting factors ranging from pollination to seed

success (Morellato et al., 2016). Discovering what shapes

Leavenworthia phenology can also help us better under-

stand phenological variation in other winter annuals.

In our study, we aimed to quantify changes over time

in Leavenworthia ﬂowering and fruiting, determine the

climatic variables and periods to which phenology was most

sensitive, and examine the relative inﬂuence of climatic

and nonclimatic factors on Leavenworthia reproductive

phenology. By analyzing 924 records spanning 117 years,

we predicted that Leavenworthia ﬂowering and fruiting have

advanced in response to warming temperatures. Given the

well‐documented but non‐uniform relationship between

climate and phenology, we also predicted that climatic

variation will have the strongest inﬂuence on ﬂowering

and fruiting dates, but with substantial variation explained

by nonclimatic factors such as self‐compatibility and

Leavenworthia species richness. To assess these predictions,

we partitioned the variance in ﬂowering and fruiting

phenology separately using a set of climatic variables

(temperature, relative humidity, precipitation, year, and

latitude) plus species‐(species, self‐compatibility) and

community‐level factors (species richness) that we expected

to inﬂuence phenology.

MATERIALS AND METHODS

Study system

Leavenworthia comprises eight nominal species that are

largely endemic to glade habitats across the southern and

southeastern United States (Figure 1). These habitats are

characterized by shallow rocky soil, limestone bedrock, and

extreme variation in local temperature and moisture

(Rollins, 1963). Individuals of the species are often found

in the areas with the shallowest soils in micro‐depressions

and seeps that retain moisture during the spring reproduc-

tive period (A. B. Smith, personal observations). Leaven-

worthia are winter annuals: seeds are dispersed during late

spring and early summer, then germinate in the fall, and

individuals overwinter as quiescent rosettes before ﬂowering

begins in the early spring (Baskin and Baskin, 1971).

Among the eight Leavenworthia species, there is high

variation in the degree of sympatry: Species diversity and

co‐occurrence are concentrated in the Central Basin of

Tennessee, while one species, L. uniﬂora, encompasses

nearly the entire range of the genus and four species have

very restricted ranges (1–4 counties for each, <2000 km

;

Koelling and Mauricio, 2010).

A notable characteristic of Leavenworthia is the

variation in self compatibility among species. While most are

self‐compatible (SC), L. stylosa is self‐incompatible, requiring

outcrossing to reproduce (Rollins, 1963;Becketal.,2006).

In L. uniﬂora,L. alabamica,andL. crassa,self‐compatibility

varies by population (Lloyd, 1965; Busch, 2005; Busch and

Werner, 2012).

Data collection

Our initial data set to assess Leavenworthia phenology

consisted of 1214 Leavenworthia herbarium records col-

lected between 1877 and 2001. This data set comprised all

specimens at 10 herbaria, which were either geographically

relevant (BRIT, IND, LL, MO, SMU, UNA, VDB) and/or

large national collections known to archive large sets of

specimens cited in Leavenworthia studies (G, NY, US)

(Rollins, 1963). At the time of compilation, we estimated

that the data set contained ~80% of all Leavenworthia

herbarium specimens. A subset of this data set was

previously used to assess phenology change in L. stylosa

(Banaszak et al., 2020).

To increase sampling from the 21st century, we

supplemented these data with Leavenworthia occurrence

records downloaded from the Global Biodiversity Informa-

tion Facility (GBIF.org, 2021;https://doi.org/10.15468/dl.

v6zf9r), including both herbarium records and iNaturalist

observations made between 2001 and 2019 (the most recent

year for which climate data were available at the time of

analysis). In total, we obtained 212 new records from GBIF

and added them to the raw data set (N= 1426).

For a sizable portion of records, the precise coordinates

of collection could not be determined due to incomplete

locality descriptions or endangered species protections. To

ensure a uniform analysis, we obtained coordinates for our

records by georeferencing each record's coordinates to the

centroid of the county in which the record was collected,

which was the ﬁnest level of spatial resolution we could

achieve across all samples. Standardizing our record

coordinates to the county level sacriﬁces a degree of detail,

speciﬁcally in relating climate data to location. However,

counties in this region inhabited by Leavenworthia have low

topographic heterogeneity, and given the characteristic

distance of spatial autocorrelation in temperature and

precipitation (several 100 km; Fick and Hijmans, 2017),

we expected the spatial autocorrelation of climate condi-

tions within a county to be high enough to not bias

our results (Getis, 2010). We excluded any records for

which the species, phenophase, date or county of collection,

self‐compatibility, or monthly climate data could not be

determined. After ﬁltering, we had 924 records.

Phenocoding

We assigned each Leavenworthia record a phenophase

based on its observed reproductive status: ﬂowering,

fruiting, both, or neither. This categorical scoring method

has been used widely (Diez et al., 2014; Davis et al., 2015;

Banaszak et al., 2020) and accurately and eﬃciently

assesses phenophase for a large number of specimens

(Pearson, 2019). Flowering was deﬁned by anthesis, or open

ﬂowering. Fruiting included both immature and mature

fruits. In cases where multiple individuals were present on

one herbarium sheet or photo, phenophase was scored

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

3of14

collectively for all present individuals. Of our 924 complete

records, 647 were scored as ﬂowering, 849 were scored as

fruiting, and 1 was scored as neither. Flowering and fruiting

co‐occurred in most specimens.

Self‐compatibility

We assigned self‐compatibility based on each record's

species and/or population. All records of L. stylosa were

designated as self‐incompatible (SI), as deﬁned by Beck

et al. (2006). All L. exigua,L. torulosa,L. aurea, and

L. texana records were designated as self‐compatible (SC),

as deﬁned by Rollins (1963) and Beck et al. (2006). Three

Leavenworthia species are known to have both SI and

SC populations: L. alabamica,L. crassa, and L. uniﬂora.

For records of these species, we attempted to assign

self‐compatibility based on subspecies, locality information,

or precise collection coordinates. All records identiﬁed as

L. alabamica var. brachystyla or L. crassa var. elongata were

assigned SC status (Lloyd, 1965). For records not identiﬁed

to subspecies, we determined the population from which the

record was collected. Busch (2005) identiﬁed selﬁng and

nonselﬁng populations of L. alabamica, listed coordinates

for each population, and named them based on nearby

localities. Where possible, we matched locality description

and/or precise collection coordinates of our L. alabamica

records to the populations outlined by Busch (2005)to

determine self‐compatibility. We did the same for L. crassa

records, according to the population names and coordinates

listed by Lloyd (1965). If the locality description or

coordinates of a record did not exactly match those

provided for a speciﬁc population, we did not attempt to

assign self‐compatibility for that record.

L. uniﬂora

Leavenworthia uniﬂora is the most widespread Leaven-

worthia species, featuring notable geographic variation in its

reproductive habits. Populations of L. uniﬂora west of the

Mississippi River self‐fertilize almost exclusively, while

eastern populations have a mixed mating system (Busch

and Werner, 2012). We conducted a t‐test using base R

(version 4.2.0, R Core Team, 2022) to determine whether

the mean day of year of L. uniﬂora reproduction diﬀered

based on population (east or west of the Mississippi

River; Appendix S1, Figure S1). However, given that both

eastern and western populations are self‐compatible and do

self‐fertilize (Beck et al., 2006; Busch and Werner, 2012), we

designated all L. uniﬂora records as SC.

Climatic data

Using the year and coordinates of each Leavenworthia

record, we obtained monthly climatic data for our records

using ClimateNA v6.40a (Wang et al., 2016), which provides

monthly‐resolution estimates of climate interpolated

across North America from 1901 to the present. Using

the coordinates for every county centroid in our data

set, we extracted monthly (1) mean temperatures, (2) total

precipitation, and (3) mean annual relative humidity (RH)

across all available and sampled years (1902–2019). We

chose these climatic variables due to their hypothesized or

empirical inﬂuence on germination and/or reproductive

phenology of Leavenworthia (Rollins, 1963; Baskin and

Baskin, 1971; Solbrig and Rollins, 1977). Keeping the

winter‐annual habit of this genus in mind, we deﬁned ﬁxed

seasonal periods in which we calculated relevant climatic

variables: the summer seed dormancy period (June–August,

in the year before collection), the fall germination

period (September–November, before collection), the win-

ter quiescent period (December of the year prior, plus

January–February of the year of collection), and the spring

reproductive period (March–May of the year of collection;

Baskin and Baskin, 1971; Banaszak et al., 2020). Mean

monthly temperature and RH were each averaged across

each climate period. Monthly precipitation was summed

across each period. Our ﬁnal data set included 647 ﬂowering

and 849 fruiting records between 1902 and 2019, each

matched with climate data corresponding to stages in the

plant's life history.

Climatic analysis

To identify the most predictive climatic variables for

inclusion in the ﬁnal variance partitioning model, we ran

two separate sets of models—one for ﬂowering and one for

fruiting with all species combined—using the lm linear

regression function in R to model the day of year (DOY) of

ﬂowering and fruiting against every possible pairwise

combination of average temperature with total precipitation

or RH, each across all four of the ﬁxed climatic periods.

Climatic variables were scaled and centered before analysis.

We compared the R

values across the resulting 32 models

in each set. The ﬂowering and fruiting models with the

highest R

in each set were used in the ﬁnal variance

partitioning analyses.

The climate variables from the most predictive models

were plotted against year to determine the change in

relevant climate over time. The most‐predictive climatic

variables were also plotted against the day of year of both

ﬂowering and fruiting to assess phenological sensitivity or

against the change in phenophase timing per unit change in

each climate variable (Davis et al., 2015). We used the sma

function in the R package smatr (version 3.4‐8; Warton

et al., 2012) to conduct one‐sample tests for diﬀerences in

slopes with all species combined between ﬂowering and

fruiting, determining whether the phenophases diﬀered in

terms of phenological sensitivity to climate (DOY vs. unit

climate) or rate of phenological change across years (DOY

vs year). We also used the sma function to test for

4of14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

diﬀerences in phenological sensitivity or rate of change

among Leavenworthia species.

To test for collinearity between climatic and the

continuous non‐climatic variables, we used the cor function

in base R, generating a matrix displaying the Peason's

correlation coeﬃcient between every possible climate

variable pair, plus year and latitude.

Variance partitioning

We conducted separate variance partitioning analyses for

ﬂowering and fruiting dates. Our ﬁnal models consisted

of a linear regression comparing the DOY of ﬂowering or

fruiting against the two climatic variables found to be most

explanatory above (mean temperature and total precipitation

during the reproductive period) and our selection of relevant

species‐(species and self‐compatibility), population‐(year

and latitude), and community‐level variables (the number of

Leavenworthia species recorded in the county of collection:

species richness), year, and latitude. All continuous variables

were scaled and centered before analysis, but species and

self‐compatibility were categorical and were thus not

transformed. To account for variation in species responses

to climate, we also included interaction terms between

species and mean reproductive temperature and between

species and total reproductive precipitation. Preliminary

models also included identity of the phenology scorer (KBB

or JBB) as a covariable to test for bias between individuals

responsible for phenophase scoring. Because scorer had no

signiﬁcant eﬀect, we dropped it from the ﬁnal models.

We ran a variance partitioning analysis on the ﬂowering

and fruiting models in R (version 4.2.0, R Core Team, 2022)

using the calc.relimp function in the relaimpo package

(version 2.2‐6; Ulrike 2006). In this procedure, all possible

subsets of models are run, then diﬀerences in R

between

models with and without a focal variable are calculated,

resulting in the total amount of R

attributable to that

variable (Chevan and Sutherland, 1991). We divided

the R

attributable to each variable by the model's total

to determine the percentage of total variance explained

attributable to each variable. Finally, we used the boot.-

relimp function to calculate 95% conﬁdence intervals

and test for signiﬁcant diﬀerences between variables via

1000 bootstrapping replicates (Fox and Monette, 2002;

Ulrike, 2006).

RESULTS

Leavenworthia ﬂowering and fruiting dates each advanced

signiﬁcantly over 117 years (Figure 2). Flowering advanced by

approximately 2.0 days per decade (slope –0.20 ± 0.02 d/yr,

=0.12,df=645,P< 0.005), while fruiting advanced approx-

imately 1.3 days per decade (slope of –0.13 ± 0.02 d/yr,

=0.04, df=847, P<0.005). Flowering date advanced

signiﬁcantly faster than fruiting (likelihood ratio = 6.46,

df = 2, P< 0.05). Species' rates of phenological change were

also signiﬁcantly diﬀerent (likelihood ratio = 54.57, df = 7,

P<0.005).

Climatic analysis

The climatic variables included in each model had

absolute values < 0.7 for Pearson's rproduct‐moment

pairwise correlations (Appendix S1, Figure S2;|r|≤0.10

for reproductive temperature and precipitation across

ﬂowering [df = 645] and fruiting [df = 847], P< 0.005 for

both), and so were not expected to confound one another

due to collinearity (Murray and Conner, 2009; Dormann

et al., 2013). Pairwise Pearson's rcorrelations between the

climatic variables, year, and latitude also fell below 0.7

(Dormann et al., 2013).

Comparing the phenological responses to 32 combinations

of climatic variables across four periods of Leavenworthia's

FIGURE 2 Flowering and fruiting day of year over time. (A) Flowering and (B) fruiting date plotted against year of collection. Each point represents a

Leavenworthia record, color‐coded by species. Colored regression lines show phenological shifts by species. Dotted black line is the best ﬁt across all records

within the genus, illustrating overall phenological change over time (ﬂowering = –0.20 ± SE 0.02 (SE) days/year; fruiting = –0.13 ± 0.02 days/year).

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

5of14

annual life history (Table 1; all 32 models ranked in

Appendix S1,TableS3), we found that average temperature

and total precipitation during the spring reproductive season

best predicted both ﬂowering date (R

= 0.287, df = 645,

P< 0.005) and fruiting date (R

= 0.294, df = 847, P<0.005).

Based on these ﬁndings, reproductive temperature and

precipitation were included as climatic variables in our ﬁnal

variance partitioning models.

We found that 1°C warming during the spring

reproductive period led to a 2.34 ± 0.35 (mean ± SE) day

advance in ﬂowering (r

= 0.06, df = 645, P< 0.005) and a

3.33 ± 0.30 day advance in fruiting (r

= 0.12, df = 847,

P< 0.005) across the genus (Figure 3). Average reproductive

season temperature in counties inhabited by Leavenworthia

increased by 0.02°C ± 0.002 per year (r

= 0.08, df = 922,

P= 0.005), or approximately 2.09°C over 117 years

(Figure 4). For a 1‐mm increase in total precipitation

during the reproductive period, ﬂowering was delayed

by 0.070 ± 0.005 days (r

= 0.23, df = 645, P< 0.005) and

fruiting by 0.060 ± 0.004 days (r

= 0.19, df = 847, P< 0.005)

(Figure 3). However, total precipitation during the repro-

ductive period decreased by ~83 mm over 117 years

(Figure 4; 0.71 mm ± 0.14 per year, r

= 0.03, df = 922,

P= 0.005).

Flowering date was signiﬁcantly more sensitive to

changes in both reproductive temperature (likelihood

ratio = 11.05, df = 2, P< 0.005) and precipitation (likelihood

ratio = 30.59, df = 2, P< 0.005) than fruiting. Species

also varied in both the direction and magnitude of their

phenological sensitivity to reproductive warming (likeli-

hood ratio = 82.71, df = 7, P< 0.005) for both ﬂowering and

fruiting (Figure 3A, B). Three species signiﬁcantly advanced

phenology: L. uniﬂora (likelihood ratio = –8.45, P< 0.005),

L. stylosa (–16.57, P< 0.005), L. exigua (–9.83, P< 0.005).

The phenology for ﬁve species had no signiﬁcant response

to spring warming—L. torulosa (–14.17, P= 0.73), L. texana

(–17.94, P= 0.32), L. alabamica (10.32, P= 0.58), L. aurea

(18.65, P= 0.51), L. crassa (16.03, P= 0.55). Species'

responses to reproductive period precipitation varied in

magnitude (likelihood ratio = 47.52, df = 7, P< 0.005), but

all advanced in response to decreasing precipitation

(Figure 3C, D).

Variance partitioning

The full models with the best climatic covariates and with all

nonclimatic covariates predicted 35.4% of total variance in

the day of year of ﬂowering (df = 619, P< 0.005), and 33.9%

of total variance in fruiting (df = 821, P< 0.005). Reproduc-

tive season precipitation was the best predictor of both

ﬂowering date and fruiting date (Figure 5). Precipitation

accounted for 51.3% of the total explained variance in

ﬂowering date (R

attributable to reproductive precipitation =

0.196, bootstrap lower and upper 95% conﬁdence intervals:

0.147, 0.246), and 44.6% of the total variance in fruiting

date (R

= 0.161, lower = 0.115 upper = 0.203). Year was the

second‐best predictor of ﬂowering date, accounting for 16.6%

of explained variance (R

= 0.063, lower = 0.037, upper =

0.097). In contrast, year only explained 5.4% of fruiting date

variance (R

= 0.019, lower = 0.007, upper = 0.036). Repro-

ductive season temperature was the second‐best predictor

of fruiting date (R

= 0.070, lower = 0.046, upper = 0.098;

19.3% of explained variance) and the third‐best predictor of

ﬂowering date (R

= 0.041, lower = 0.021, upper = 0.070;

10.6% of explained variance). Latitude was the third‐best

TABLE 1 Flowering and fruiting models ranked by R

. Flowering and fruiting dates were modeled against every two‐variable combination of mean

temperature, mean relative humidity, and total precipitation across four seasons (germination, September–November; quiescent, December–February;

reproductive, Mar–May; and dormancy, June–August). The ﬁve best‐predictive ﬂowering models and the ﬁve best‐predictive fruiting models are listed

above, ranked from highest R

to lowest R

. The climate variables from the best‐predictive models were used with nonclimatic variables in the variance

partitioning analyses.

Model Temperature slope (±SE) Moisture slope (±SE) R

Flowering

Reproductive temperature + Reproductive precipitation –3.36 ± 0.46 6.49 ± 0.46 0.287

Quiescent temperature + Reproductive precipitation –2.48 ± 0.48 5.91 ± 0.48 0.258

Germination temperature + Reproductive precipitation –2.16 ± 0.47 6.55 ± 0.47 0.252

Dormancy temperature + Reproductive precipitation –1.42 ± 0.47 6.54 ± 0.47 0.238

Quiescent temperature + Germination relative humidity (RH) −4.27 ± 0.50 –3.22 ± 0.50 0.139

Fruiting

Reproductive temperature + Reproductive precipitation –4.62 ± 0.42 5.96 ± 0.42 0.294

Quiescent temperature + Reproductive precipitation –3.87 ± 0.45 5.25 ± 0.45 0.259

Germination temperature + Reproductive precipitation –3.53 ± 0.43 6.32 ± 0.43 0.252

Dormancy temperature + Reproductive precipitation –2.67 ± 0.44 6.31 ± 0.44 0.227

Quiescent temperature + Germination precipitation –5.41 ± 0.45 –2.46 ± 0.45 0.166

6of14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

predictor of fruiting date (R= 0.054, lower = 0.036, upper =

0.076; 15.1% of explained variance) but had nominal

inﬂuence on ﬂowering. Interactions between species identity

and climate aﬀected ﬂowering more than fruiting (total R

from interactions = 0.05 or 13.8% of total explained ﬂowering

variance vs. R

= 0.02 or 5.1% of fruiting).

According to our bootstrap analysis, reproductive precip-

itation explained signiﬁcantly more ﬂowering and fruiting

variance than any other variable. Nonclimatic factors (species,

richness, and self‐compatibility) combined were compara-

tively weak predictors, accounting for only 5.3% of explained

ﬂowering variance and 10.5% of fruiting (Figure 5).

L. uniﬂora

We found signiﬁcant phenological diﬀerences between

eastern and western populations of L. uniﬂora (t=–4.26,

df = 155.46, P< 0.005; Appendix S1, Figure S1). The eastern

population of L. uniﬂora had a mean reproductive day of

year of 102, while the mean day of year in the western

population was 111. However, given that both species

identity collectively explained comparatively little pheno-

logical variance, we chose not to incorporate eastern vs

western population as an additional variable in our variance

partitioning models.

DISCUSSION

In this study of phenological changes within the genus

Leavenworthia and the relative inﬂuence of climatic and

nonclimatic factors on ﬂowering and fruiting dates, total

spring precipitation best predicted both ﬂowering and

fruiting dates. Variables of secondary importance included

year, reproductive temperature, and interactions between

FIGURE 3 Sensitivity of Leavenworthia ﬂowering and fruiting date to reproductive period climate. (A, C) Flowering and (B, D) fruiting date plotted

against mean temperature (A, B) and total precipitation (C, D) during the spring reproductive period (March–May). Each point represents a Leavenworthia

record, color‐coded by species. Colored regression lines demonstrate species phenological responses to changes in temperature and precipitation. Dotted

black line is the best ﬁt across all Leavenworthia records, illustrating mean phenological sensitivity across the genus to spring warming (–2.3 ± 0.35 days/°C

for ﬂowering; –3.3 ± 0.30 days/°C for fruiting) or drying (–0.07 ± 0.004 days/mm for ﬂowering; –0.06 ± 0.004 days/mm for fruiting).

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

7of14

species and precipitation for ﬂowering and between

reproductive temperature and latitude for fruiting. These

results align with numerous studies that found that shifts in

climatic cues prompt changes in plant phenology (e.g.,

Miller‐Rushing and Primack, 2008; Wilczek et al., 2010;

Banaszak et al., 2020; Love and Mazer, 2021). We found that

a 100‐mm decrease in spring precipitation was correlated

with a 7‐day advance in ﬂowering and 6‐day advance in

fruiting. For every 1°C of spring warming, Leavenworthia

ﬂowering and fruiting advanced by more than 2 days,

although there was signiﬁcant variation between species.

Over our 117‐year study period, springtime temperature in

areas inhabited by Leavenworthia increased by 2.09°C,

while spring precipitation declined by ~83 mm. As a result,

Leavenworthia reproduction has advanced by approximately

2 weeks. Nonclimatic factors (species, self‐compatibility,

and species richness) explained the lowest proportion of the

total phenological variance.

Phenological predictors and trends

This study is one of the few to assess diﬀerences in

phenological shifts across an entire genus (e.g., Debussche

et al., 2004). While phenological advances in a single

Leavenworthia species—L. stylosa—have been previously

reported (Banaszak et al., 2020), ours is the ﬁrst to quantify

climatic sensitivity and the rate of phenological change

for all Leavenworthia. Our results somewhat contrast

with previous work on L. stylosa, which found advanced

phenology in response to local cooling and increased

precipitation using a subset of the same herbarium data

used here (Banaszak et al., 2020). We and Banaszak et al.

(2020) found a comparable rate of advancement (1–2 days

per decade); in our study, however, this phenological

advance is linked to spring warming and drying across

the range of the genus, rather than to year‐round cooling

within the restricted region examined by Banaszak et al.

(2020). We did ﬁnd, however, that Leavenworthia species

varied signiﬁcantly in their rates of phenological advance

and climate sensitivities, with three species (L. aurea,

L. alabamica, and L. crassa) not responsive to warming.

Additionally, diﬀerences in the spatial and temporal

resolution of climatic data may account for the diﬀering

results between our study and Banaszak et al. (2020). We

found signiﬁcant diﬀerences between ﬂowering and fruiting

in terms of the rate of phenological shifts (days per year)

and phenological sensitivity to climate (days per unit

climate). Additionally, our variance partitioning revealed

notable diﬀerences in the factors best explaining variance in

ﬂowering versus fruiting dates. Flowering and fruiting

are distinct phenophases, and shifts in their timing can

create distinct evolutionary and ecological consequences.

While shifts in ﬂowering time may aﬀect coﬂowering and

pollination dynamics (Elzinga et al., 2007; Sherry et al., 2007;

Kehrberger and Holzschuh, 2019; Rudolf, 2019), a change in

fruiting time aﬀects the conditions to which seeds are

exposed, ultimately shaping dispersal, dormancy length, and

germination times (Lacey et al., 2003; Vergara‐Tabares

et al., 2016; Du et al., 2020). We found that temperature

and latitude explained a greater portion of fruiting variance

than ﬂowering. Baskin and Baskin (1971) documented a

temperature‐sensitive seed dormancy that varies with seed

age in L. torulosa,L. stylosa, and L. uniﬂora. The sensitivity

of fruiting time to temperature could be a mechanism to

control the conditions to which seed is exposed, which in

turn shapes seed dormancy and aﬀects the likelihood of

germination. Determining the speciﬁc factors that shape

FIGURE 4 Change in reproductive season climate over 117 years. Mean temperature (A) and total precipitation (B) during the spring reproductive

season (March–May) plotted against year. Each dot represents the calculated spring climate for a single Leavenworthia record. Blue lines are best ﬁt across all

records, demonstrating change in temperature (0.02 ± 0.35°C/year, P< 0.005) and precipitation (–0.71 ± 0.14 mm/year, P< 0.005) over time. Gray shading

illustrates standard error.

8of14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

diﬀerent reproductive events helps to better understand the

implications of phenology shifts going forward.

Inﬂuence of climate

Total precipitation during the spring reproductive period

(March–May) was the strongest predictor of both ﬂowering

and fruiting times. This window of sensitivity coincides with

ﬂowering and fruiting dates of the majority of specimens in

our data set (Appendix S1, Figure S4) and aligns with a

multitude of studies suggesting that spring climatic condi-

tions have an impact on the reproductive phenology of

plants (Miller‐Rushing and Primack, 2008; Lesica and

Kittelson, 2010; Cook et al., 2012a,b) including winter

annuals (Banaszak et al., 2020) and range‐limited species

(Zettlemoyer et al., 2021).

The outsized inﬂuence of spring precipitation com-

pared to temperature is of note. While ﬂowering and

fruiting dates were positively correlated with reproductive

season precipitation, spring precipitation has actually

decreased over time. Accordingly, Leavenworthia phenol-

ogy has advanced. This sensitivity to spring moisture

could be at least partially attributed to the preference of

Leavenworthia for limestone prairies and barrens, or

glades. Moisture varies widely in the shallow glade soils,

ranging from extremely dry in the summers to fully

saturated by the early spring (Kucera and Martin, 1957;

Rollins, 1963). Given this high intra‐annual variability,

Leavenworthia is likely highly sensitive to moisture

changes during the reproductive period. The strong

inﬂuence of spring precipitation aligns with previous

Leavenworthia studies, which found that phenological

response to temperature and moisture throughout the

year depends speciﬁcally on reproductive season precipi-

tation (Banaszak et al., 2020). Banaszak et al. (2020) noted

that in years when fall and winter were wetter and spring

was warmer and drier, ﬂowering of L. stylosa advanced.

Wedetectedthesesameclimatictrends—increased fall

and winter precipitation (Appendix S1,FigureS5),

decreased spring precipitation, and increased spring

temperature—across the range of the genus since 1902.

Our results add to the growing body of literature

highlighting the strong but complex eﬀect of precipitation

on phenology, where changes in moisture interact with

temperature to produce varied and unexpected phenolog-

ical changes (Ganjurjav et al., 2020; Zettlemoyer

et al., 2021; Currier and Sala, 2022).

Spring temperature was also an important predictor of

Leavenworthia phenology, accounting for the second

highest proportion of fruiting variance and third

highest proportion of ﬂowering variance. Rising spring

temperatures have been widely associated with advanced

phenology (Menzel et al., 2006; Miller‐Rushing and

Primack, 2008; Lesica and Kittelson, 2010;Yuetal.,2010;

Cook et al., 2012b), especially in spring‐ﬂowering species.

However, Leavenworthia species varied signiﬁcantly in

their responses to warming spring temperature, with three

species signiﬁcantly advancing phenology (L. uniﬂora,

L. stylosa, L. exigua, L. torulosa,L. texana)andﬁve species

phenologically nonresponsive (L. aurea,L. alabamica,

L. crassa,L. torulosa,andL. texana). Earlier studies on the

genus (Baskin and Baskin, 1971)revealedthatL. aurea,

endemic to southeastern Oklahoma, varied from more

northern and eastern species in their seed dormancy and

temperature requirements for germination. The species

least responsive to warming are experiencing the same

climatic trends across seasons as those with advanced

phenology—spring warming and drying and winter

warming and wetting. However, with the exception of

L. torulosa, these species are some of the southernmost in

the genus. The warmer baseline temperatures may shape

the responses of these species to warming. Additionally,

these are some of the more range‐limited species in the

FIGURE 5 Variance partitioned in Leavenworthia (A) ﬂowering and

(B) fruiting dates. The total variance explained by our ﬂowering (A) and

fruiting (B) models, partitioned by variable. Bars indicate the proportion of

model variance explained by each variable. Asterisks indicate variables that

explain signiﬁcant portions of variance. The ﬂowering model explained

35.4% of phenological variance (df = 619, P< 0.005) and the fruiting model

explained 33.9% of variance (df = 821, P<0.005). Variables include the

temperature and moisture variables of the life stage with greatest

explanatory power, species identity, county‐level Leavenworthia species

richness, and latitude and year of each record.

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

9of14

genus. When compared to widespread relatives, extirpated

plant species have been shown to have more variable

responses to spring warming than their extant counter-

parts (Zettlemoyer et al., 2021). Given the variation

detected between species' ﬂowering and fruiting times,

future work could also explore whether seasonality (e.g.,

early‐vs. late‐ﬂowering) aﬀects phenological sensitivity

to changes in climate. Overall, our results illustrate

signiﬁcant intrageneric variation in phenological sensitiv-

ity to climate and that phenological uniformity in related

species should not be assumed.

Factors correlated with climate

Year of collection was the second‐most explanatory

variable predicting ﬂowering date, explaining marginally

more variation than spring temperature. The unique

inﬂuence of year on ﬂowering date, as opposed to a

speciﬁc climatic variable, could be attributed to a variety

of factors. Year was not highly correlated with the climatic

variables used in our models (Appendix S1,FigureS2,

|r| < 0.26); yet, year could explain a high proportion of

phenological variance because it encompasses climatic

conditions across all seasons, rather than a single period.

Various studies indicate that climate during the fall and/or

winter period can also exert a strong inﬂuence on spring

ﬂowering time (Miller‐Rushing and Primack, 2008;Cook

et al., 2012a; Zettlemoyer et al., 2021) including in winter

annuals (Wilczek et al., 2010)andLeavenworthia in

particular (Banaszak et al., 2020). In our analysis, the

combination of winter quiescent temperature and spring

reproductive precipitation was the second‐best model for

predicting ﬂowering and fruiting date (Table 1). The

inclusion of winter climatic changes over time within

“year”could explain the variable's relatively high predic-

tive power. Other climatic cues, that were not included

here but which are correlated with year, could also shape

ﬂowering time. In the preliminary analyses, we assessed

multiple climatic periods and variables beyond basic

measures of temperature and precipitation, speciﬁcally

relative humidity. While humidity did not outperform

total precipitation as a phenological predictor, other

environmental cues that act more directly yet are not

traditionally tested, such as soil temperature or moisture,

could have an impact on phenology. Year could also be

confounded with herbarium biases such as collection

eﬀort (Daru et al., 2017), or other phenologically relevant

factors, such as community composition, competition, or

rates of disease and parasitism that may vary temporally.

Latitude of collection was the third‐most predictive

variable in our fruiting model, explaining signiﬁcantly more

variance in fruiting date than year and nonclimatic factors.

Latitude was not highly correlated with the climatic variables

included here (|r| < 0.7; Appendix S1, Figure S2). The

stronger inﬂuence of latitude over year of collection could

indicate that, compared to ﬂowering, changing climate over

time has had a smaller impact on Leavenworthia fruiting.

Instead, diﬀerences in temperature or photoperiod

across a latitudinal gradient may be stronger determinants

of fruiting date. Complex interactions between temperature,

precipitation, and photoperiod shape both vegetative and

reproductive phenology (Legros et al., 2009; Müller and

Schmidt, 2018; Du et al., 2020). For example, photoperiod

can moderate leaf‐out date in temperate trees to prevent

excessively early or late leaf‐out due to temperature

ﬂuctuations (Meng et al., 2021). Photoperiod could exert a

similar eﬀect on Leavenworthia fruiting.

Nonclimatic factors

We expected to ﬁnd that nonclimatic factors—self‐

compatibility, species, and species richness in the county

of collection—would predict a signiﬁcant amount of the

phenological variance in Leavenworthia. However, we found

that nonclimatic variables accounted for very little of the

total variance explained by our models. These result suggest

that climatic changes are eliciting a similar phenological

response across Leavenworthia, regardless of species,

self‐compatibility, or intrageneric competition—aﬁnding

that suggests strong phylogenetic niche conservatism in

Leavenworthia phenology (Wiens, 2007; Wiens et al., 2010).

Evolutionary history may inﬂuence phenological variance,

but due to the number of species in the genus we were

unable to test for this here.

Conservation

While only one Leavenworthia species—L. crassa—is

federally listed under the U.S. Endangered Species Act

(U.S. Fish and Wildlife Service, 2020), four of the eight

species in the genus—L. crassa,L. alabamica,L. aurea, and

L texana—meet the NatureServe criteria for “imperiled”or

“critically imperiled”(NatureServe, 2022). These species are

habitat specialists on spatially restricted glades, which are

threatened by diverse factors such as agricultural develop-

ment, road maintenance, mining and oil extraction, and

invasive species (NatureServe, 2022).

Even barring complete habitat destruction, changes

in climate likely will create an uncertain future for the

genus. Because Leavenworthia and other glade specialists

already possess adaptations to extreme heat and aridity, it

is possible that the impact of climatic changes is negligible

(Miller‐Struttmann, 2011;Brandtetal.,2014). However,

our study demonstrates that Leavenworthia phenology is,

in fact, sensitive to changes in temperature—aﬁnding in

line with other glade specialists (Miller‐Struttmann, 2011)

and range‐limited species (Zettlemoyer et al., 2021)being

more phenologically responsive to climate than their

generalist relatives. The limited seed dispersal ability and

speciﬁc habitat preferences of species in the genus

(Rollins, 1963) restrict their capacity for migration,

10 of 14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

meaning that Leavenworthia species will most likely have

to adapt in place to changing climate. The advanced

phenology could have an impact on the success of

Leavenworthia reproduction. For example, Baskin and

Baskin (1971) found that young seeds (0–1 month old) will

only germinate at or below 15°C; with age, however (3–5

months old), seeds will germinate at temperatures as high

as 25°C. This dynamic dormancy works well when seed

sets in May: optimal germination temperatures generally

do not match ambient temperatures until the early fall,

when seedlings are most likely to successfully establish. We

found, however, that the majority of Leavenworthia

fruiting now occurs in April. If fruiting continues to

advance, seeds could be 3–5monthsoldasearlyasJuneor

July, causing higher maximum germination temperatures

to coincide with high ambient temperatures, which could

increase the number of Leavenworthia germinating in the

summer and decrease seedling establishment (Baskin and

Baskin, 1971). Ultimately, if advanced phenology of

Leavenworthia in response to spring climate creates such

barriers to reproduction, this advancement, in combina-

tion with habitat destruction, could have serious

conservation implications for this imperiled genus

(Cartwright, 2019). However, the ﬁtness and viability

impacts of changing phenology vary widely (Miller‐

Rushing et al., 2010; Willis et al., 2010; Iler et al., 2019),

and more research is required to determine the speciﬁc

implications of Leavenworthia phenology shifts within

glade habitats. More broadly, glade habitats are home to a

disproportionate number of the region's endemic species

(Ware, 2002; Zollner et al., 2005). Since these other species

experience the same general climate and threats as

Leavenworthia, our results suggest that they may also be

experiencing changes in reproductive phenology, with

similar consequences for their long‐term viability.

CONCLUSIONS

We demonstrated that Leavenworthia ﬂowering and fruit-

ing dates advanced signiﬁcantly across 117 years, largely

due to climatic factors including spring precipitation and

temperature. A notable portion of variance in ﬂowering was

also explained by year and in fruiting by latitude. By

assessing phenological change at the genus level, we utilized

a unique approach for determining the factors aﬀecting

plant reproductive phenology and demonstrated signiﬁcant

interspeciﬁc phenological variance. This study contributes

to a narrow body of literature on phenological variation

with genera (e.g., Debussche et al., 2004) and supports

climate as the dominant factor inﬂuencing reproductive

timing. Our study also demonstrates the importance of

separating ﬂowering and fruiting phenophases when testing

for factors inﬂuencing phenology. We found that ﬂowering

and fruiting times changed at diﬀerent rates, were primarily

determined by diﬀerent climate‐associated factors, and

varied in their phenological sensitivity to spring warming.

We presented long‐term data on the reproductive habits

and sensitivities of a highly imperiled genus, with broad

implications for future phenological research under con-

tinuing climatic changes.

AUTHOR CONTRIBUTIONS

K.B.: Conceptualization (equal); investigation (lead); formal

analysis (equal); original draft preparation (lead).

M.A.: conceptualization (equal); investigation (supporting);

review and editing (equal). J.B.: investigation (supporting);

review and editing (equal). A.Z.: formal analysis (equal);

supervision (equal); review and editing (equal). A.S.:

conceptualization (equal); methodology (lead); supervision

(equal); review and editing (equal).

ACKNOWLEDGMENTS

We thank the Shirley A. Graham Fellowship and the Alan

Graham Fund in Global Change of the Missouri Botanical

Garden for funding to support this project. We thank our

reviewers for their helpful feedback shaping this manuscript.

We thank Ihsan Al‐Shehbaz of the Missouri Botanical

Garden for help with Leavenworthia taxonomy. We also

thank the Global Change & Conservation and Zanne Labs for

manuscript feedback and the hundreds of botanical collectors

and community scientists for documenting Leavenworthia.

DATA AVAILABILITY STATEMENT

All data and code used in our analysis are available at the Dryad

Digital Repository: https://doi.org/10.5061/dryad.70rxwdc3f.

The speciﬁcGBIFsearchusedtoacquireLeavenworthia records

is available at https://doi.org/10.15468/dl.v6zf9r.

ORCID

Kelsey B. Bartlett http://orcid.org/0000-0001-8154-5261

Matthew W. Austin http://orcid.org/0000-0002-

1231-9081

James B. Beck http://orcid.org/0000-0003-4052-6077

Amy E. Zanne https://orcid.org/0000-0001-6379-9452

Adam B. Smith https://orcid.org/0000-0002-6420-1659

REFERENCES

Al‐Shehbaz, I. A., and J. B. Beck. 2010. Leavenworthia. In. Flora of North

America Editorial Committee [eds.], Flora of North America north of

Mexico, vol. 7, 485–489. Oxford University Press, NY, NY, USA.

Austin, M. W., P. O. Cole, K. M. Olsen, and A. B. Smith. 2022. Climate

change is associated with increased allocation to potential outcrossing

in a common mixed mating species. American Journal of Botany 109:

1085–1096.

Banaszak, C., J. B. Grinath, and C. R. Herlihy. 2020. Chilling consequences:

Herbarium Records reveal earlier reproductive phenology of winter

annual gladecress in a wetter, cooler climate. Plants, People, Planet 2:

340–352.

Bartomeus, I., J. S. Ascher, D. Wagner, B. N. Danforth, S. Colla,

S. Kornbluth, and R. Winfree. 2011. Climate‐associated phenological

advances in bee pollinators and bee‐pollinated plants. Proceedings of

the National Academy of Sciences, USA 108: 20645–20649.

Barve, V. V., L. Brenskelle, D. Li, B. J. Stucky, N. V. Barve, M. M. Hantak,

B. S. McLean, et al. 2020. Methods for broad‐scale plant phenology

assessments using citizen scientists' photographs. Applications in

Plant Sciences 8: e11315.

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

11 of 14

Baskin, C. C., and J. M. Baskin. 1971. Seeds: ecology, biogeography and

evolution of dormancy and germination. Academic Press, San Diego,

CA, USA.

Beck, J. B., I. A. Al‐Shehbaz, and B. A. Schaal. 2006. Leavenworthia

(Brassicaceae) revisited: testing classic systematic and mating system

hypotheses. Systematic Botany 31: 151–159.

Belitz, M. W., E. A. Larsen, L. Ries, and R. P. Guralnick. 2020. The

accuracy of phenology estimators for use with sparsely sampled

presence‐only observations. Methods in Ecology and Evolution 11:

1273–1285.

Brandt, L., H. He, L. Iverson, F. R. Thompson III, P. Butler, S. Handler,

M. Janowiak, et al. 2014. Central Hardwoods ecosystem vulnerability

assessment and synthesis: a report from the Central Hardwoods

Climate Change Response Framework project. General Technical

Report NRS‐124. U.S. Department of Agriculture, Forest Service,

Northern Research Station, Newtown Square, PA, USA. Website:

https://doi.org/10.2737/NRS-GTR-124

Brearley, F. Q., J. Proctor, L. Nagy, G. Darlrymple, and B. C. Voysey. 2007.

Reproductive phenology over a 10‐year period in a lowland evergreen

rain forest of central Borneo. Journal of Ecology 95: 828–839.

Busch, J. W. 2005. Inbreeding depression in self‐incompatible and

self‐compatible populations of Leavenworthia alabamica.Heredity 94:

159–165.

Busch, J. W., C. R. Herlihy, L. Gunn, and W. J. Werner. 2010. Mixed

mating in a recently derived self‐compatible population of

Leavenworthia alabamica (Brassicaceae). American Journal of

Botany 97: 1005–1013.

Busch, J. W., and W. J. Werner. 2012. Population structure has limited

ﬁtness consequences in the highly selﬁng plant Leavenworthia

uniﬂora (Brassicaceae). International Journal of Plant Sciences 173:

495–506.

Campbell, D. R. 1985a. Pollen and gene dispersal: the inﬂuences of

competition for pollination. Evolution 39: 418–431.

Campbell, D. R. 1985b. Pollinator sharing and seed set of Stellaria pubera:

competition for pollination. Ecology 66: 544–553.

Cartwright, J. 2019. Ecological islands: conserving biodiversity hotspots in

a changing climate. Frontiers in Ecology and the Environment 17:

331–340.

Chevan, A., and M. Sutherland. 1991. Hierarchical partitioning. American

Statistician 45: 90–96.

Cole, E. F., and B. C. Sheldon. 2017. The shifting phenological landscape:

within‐and between‐species variation in leaf emergence in a mixed‐

deciduous woodland. Ecology and Evolution 7: 1135–1147.

Cook, B. I., E. M. Wolkovich, and C. Parmesan. 2012a. Divergent responses

to spring and winter warming drive community level ﬂowering

trends. Proceedings of the National Academy of Sciences, USA 109:

9000–9005.

Cook, B. I., E. M. Wolkovich, T. J. Davies, T. R. Ault, J. L. Betancourt,

J. M. Allen, K.Bolmgren, et al. 2012b. Sensitivity of spring phenology

to warming across temporal and spatial climate gradients in two

independent databases. Ecosystems 15: 1283–1294.

Currier, C. M., and O. E. Sala. 2022. Precipitation versus temperature as

phenology controls in drylands. Ecology 103: e3793.

Daru, B. H., D. S. Park, R. B. Primack, C. G. Willis, D. S. Barrington,

T. J. Whitfeld, T. G. Seidler, et al. 2017. Widespread sampling biases

in herbaria revealed from large‐scale digitization. New Phytologist

217: 939–955.

Davis, C. C., C. G. Willis, B. Connolly, C. Kelly, and A. M. Ellison. 2015.

Herbarium records are reliable sources of phenological change

driven by climate and provide novel insights into species'

phenological cueing mechanisms. American Journal of Botany 102:

1599–1609.

Debussche, M., E. Garnier, J. D. Thompson. 2004. Exploring the causes of

variation in phenology and morphology in Mediterranean geophytes:

a genus‐wide study of Cyclamen.Botanical Journal of the Linnean

Society 145: 469–484.

Dormann, C. F., J. Elith, S. Bacher, C. Buchmann, G. Carl, G. Carré,

J. R. G. Marquéz, et al. 2013. Collinearity: a review of methods to

deal with it and a simulation study evaluating their performance.

Ecography 36: 27–46.

Du, Y., L. Mao, S. A. Queenborough, R. Primack, L. S. Comita, A. Hampe,

and K. Ma. 2020. Macro‐scale variation and environmental predictors

of ﬂowering and fruiting phenology in the Chinese angiosperm ﬂora.

Journal of Biogeography 47: 2303–2314.

Elzinga, J. A., A. Atlan, A. Biere, L. Gigord, A. E. Weis, and G. Bernasconi.

2007. Time after time: ﬂowering phenology and biotic interactions.

Trends in Ecology & Evolution 22: 432–439.

Fick, S. E., and R. J. Hijmans. 2017. WorldClim 2: New 1‐km spatial

resolution climate surfaces for global land areas. International Journal

of Climatology 37: 4302–4315.

Fox, J. 2002. Bootstrapping regression models. In An R and S‐PLUS

companion to applied regression, 1–14. SAGE, Thousand Oaks,

CA, USA.

Ganjurjav,H.,E.S.Gornish,G.Hu,M.W.Schwartz,Y.Wan,Y.Li,and

Q. Gao. 2020. Warming and precipitation addition interact to aﬀect

plant spring phenology in alpine meadows on the central Qinghai‐

Tibetan plateau. Agricultural and Forest Meteorology 287: 107943.

Gavini, S. S., A. Sáez, C. Tur, and M. A. Aizen. 2021. Pollination success

increases with plant diversity in high‐Andean communities. Scientiﬁc

Reports 11: 22107.

GBIF.org. 2021. GBIF occurrence download. Website: https://doi.org/10.

15468/dl.v6zf9r

Getis, A. 2010. Spatial autocorrelation. In M. Fischer and A. Getis [eds.],

Handbook of applied spatial analysis. Springer, Berlin, Germany.

Gorman,C.E.,L.Bond,M.vanKleunen,M.E.Dorken,andM.Stift.

2020. Limited phenological and pollinator‐mediated isolation

among selﬁng and outcrossing Arabidopsis lyrata populations.

Proceedings of the Royal Society, B, Biological Sciences. 287:

20202323.

Harrison, M. E., N. Zweifel, S. J. Husson, S. M. Cheyne, L. J. D'Arcy,

F. A. Harsanto, H. C. Morrogh‐Bernard, et al. 2015. Disparity in

onset timing and frequency of ﬂowering and fruiting events in two

Bornean peat‐swamp forests. Biotropica 48: 188–197.

Hart,R.,J.Salick,S.Ranjitkar,andJ.Xu.2014.Herbariumspecimens

show contrasting phenological responses to Himalayan climate.

Proceedings of the National Academy of Sciences, USA 111:

10615–10619.

Iler, A. M., A. Compagnoni, D. W. Inouye, J. L. Williams, P. J. CaraDonna,

A. Anderson, and T. E. Miller. 2019. Reproductive losses due to

climate change‐induced earlier ﬂowering are not the primary threat

to plant population viability in a perennial herb. Journal of Ecology

107: 1931–1943.

Iwanycki Ahlstrand, N., R. B. Primack, and A. P. Tøttrup. 2022. A

comparison of herbarium and citizen science phenology datasets for

detecting response of ﬂowering time to climate change in Denmark.

International Journal of Biometeorology 66: 849–862.

Kehrberger, S., and A. Holzschuh. 2019. How does timing of ﬂowering

aﬀect competition for pollinators, ﬂower visitation and seed set in an

early spring grassland plant? Scientiﬁc Reports 9: 1–9.

Koelling, V. A., and R. Mauricio. 2010. Genetic factors associated with

mating system cause a partial reproductive barrier between two

parapatric species of Leavenworthia (Brassicaceae). American Journal

of Botany 97: 412–422.

Kucera, C. L., and S. C. Martin. 1957. Vegetation and soil relationships in

the glade region of the southwestern Missouri Ozarks. Ecology 38:

285–291.

Lacey, E. P., D. A. Roach, D. Herr, S. Kincaid, and R. Perrott. 2003.

Multigenerational eﬀects of ﬂowering and fruiting phenology in

Plantago lanceolata.Ecology 84: 2462–2475.

Legros, S., I. Mialet‐Serra, J.‐P. Caliman, F. A. Siregar, A. Clément‐Vidal,

and M. Dingkuhn. 2009. Phenology and growth adjustments of oil

palm (Elaeis guineensis) to photoperiod and climate variability.

Annals of Botany 104: 1171–1182.

Lesica, P., and P. M. Kittelson. 2010. Precipitation and temperature are

associated with advanced ﬂowering phenology in a semi‐arid

grassland. Journal of Arid Environments 74: 1013–1017.

12 of 14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

Lloyd, D. G. 1965. Evolution of self‐compatibility and racial diﬀerentiation

in Leavenworthia (Cruciferae). Contributions from the Gray

Herbarium of Harvard University 195: 3–134.

Love, N. L., and S. J. Mazer. 2021. Region‐speciﬁc phenological sensitivities

and rates of climate warming generate divergent temporal shifts in

ﬂowering date across a species' range. American Journal of Botany

108: 1873–1888.

Mazer,S.J.,N.L.Love,I.W.Park,T.Ramirez‐Parada, and

E. R. Matthews. 2021. Phenological sensitivities to climate are

similar in two Clarkia congeners: indirect evidence for facilitation,

convergence, niche conservatism, or genetic constraints. Madroño

68: 388–405.

Meineke, E. K., C. C. Davis, and T. J. Davies. 2018. The unrealized potential

of herbaria for global change biology. Ecological Monographs 88:

505–525.

Meng, L., Y. Zhou, L. Gu, A. D. Richardson, J. Peñuelas, Y. Fu, Y. Wang,

et al. 2021. Photoperiod decelerates the advance of spring phenology

of six deciduous tree species under climate warming. Global Change

Biology 27: 2914–2927.

Menzel,A.,T.H.Sparks,N.Estrella,E.Koch,A.Aasa,R.Ahas,K.Alm‐

Kübler, et al. 2006. European phenological response to climate

change matches the warming pattern. Global Change Biology 12:

1969–1976.

Miller‐Rushing, A. J., and R. B. Primack. 2008. Global warming and

ﬂowering times in Thoreau's Concord: a community perspective.

Ecology 89: 332–341.

Miller‐Rushing, A. J., T. T. Høye, D. W. Inouye, and E. Post. 2010. The

eﬀects of phenological mismatches on demography. Philosophical

Transactions of the Royal Society, B, Biological Sciences 365:

3177–3186.

Miller‐Struttmann, N. 2011. Causes of rarity in glade‐endemic plants:

Implications for responses to climate change. Ph.D. dissertation,

Washington University, St. Louis, MO, USA.

Morellato, L. P., B. Alberton, S. T. lvarado, B. Borges, E. Buisson,

M. G. Camargo, L. F. Cancian, et al. 2016. Linking plant phenology to

conservation biology. Biological Conservation 195: 60–72.

Munguía‐Rosas, M. A., J. Ollerton, V. Parra‐Tabla, and J. A. De‐Nova.

2011. Meta‐analysis of phenotypic selection on ﬂowering phenology

suggests that early ﬂowering plants are favored. Ecology Letters 14:

511–521.

Müller, A., and J. L. Schmitt. 2018. Phenology of Guarea macrophylla Vahl

(Meliaceae) in subtropical riparian forest in southern Brazil. Brazilian

Journal of Biology 78: 187–194.

Murray, K., and M. M. Conner. 2009. Methods to quantify variable

importance: Implications for the analysis of noisy ecological data.

Ecology 90: 348–355.

NatureServe. 2022. NatureServe Explorer [web application], NatureServe

Network Biodiversity Location Data. NatureServe, Arlington,

VA,USA.Website:https://explorer.natureserve.org/ [accessed 21

July 2022].

Parmesan, C. 2006. Ecological and evolutionary responses to recent climate

change. Annual Review of Ecology, Evolution, and Systematics 37:

637–669.

Pearson, K. D. 2019. A new method and insights for estimating

phenological events from herbarium specimens. Applications in

Plant Sciences 7: e01224.

Pemadasa, M. A., and P. H. Lovell. 1974. Factors controlling the ﬂowering

time of some dune annuals. Journal of Ecology 62: 869–880.

Piao, S., Q. Liu, A. Chen, I. A. Janssens, Y. Fu, J. Dai, L. Liu, et al. 2019.

Plant phenology and global climate change: current progresses and

challenges. Global Change Biology 25: 1922–1940.

R Core Team. 2022. R: a language and environment for statistical

computing. R Foundation for Statistical Computing, Vienna, Austria.

Website: https://www.R-project.org/

Raﬀerty, N. E., and P. D. Nabity. 2017. A global test for phylogenetic signal

in shifts in ﬂowering time under climate change. Journal of Ecology

105: 627–633.

Rollins, R. C. 1963. The evolution and systematics of Leavenworthia

(Cruciferae). Contributions from the Gray Herbarium of Harvard

University 192: 3–98.

Rudolf, V. H. 2019. The role of seasonal timing and phenological shifts for

species coexistence. Ecology Letters 22: 1324–1338.

Shen, M., S. Piao, N. Cong, G. Zhang, and I. A. Jassens. 2015. Precipitation

impacts on vegetation spring phenology on the Tibetan Plateau.

Global Change Biology 21: 3647–3656.

Sherry, R. A., X. Zhou, S. Gu, J. A. Arnone, D. S. Schimel, P. S. Verburg,

L. L. Wallace, and Y. Luo. 2007. Divergence of reproductive

phenology under climate warming. Proceedings of the National

Academy of Sciences, USA 104: 198–202.

Solbrig, O. T., and R. C. Rollins 1977. The evolution of autogamy in species

of the mustard genus Leavenworthia.Evolution 31: 265–281.

Stone, G. N., P. Willmer, and J. A. Rowe. 1998. Partitioning of pollinators

during ﬂowering in an African acacia community. Ecology 79:

2808–2827.

Suonan,J.,A.T.Classen,Z.Zhang,andJ.S.He.2017.Asymmetricwinter

warming advanced plant phenology to a greater extent than symmetric

warminginanalpinemeadow.Functional Ecology 31: 2147–2156.

Ulrike, G. 2006. Relative importance for linear regression in R: the package

relaimpo. Journal of Statistical Software 17: 1–27.

U.S. Fish and Wildlife Service. 2020. Fleshy‐fruit gladecress (Leavenworthia

crassa)5‐year review: summary and evaluation. U.S. Fish and

Wildlife Service, South Atlantic‐Gulf Region, Alabama Ecological

Services Field Oﬃce. Website: https://ecos.fws.gov/docs/ﬁve_year_

review/doc6775.pdf [accessed 8 June 2022].

Vergara‐Tabares, D. L., J. Badini, and S. I. Peluc. 2016. Fruiting phenology

as a “triggering attribute”of invasion process: Do invasive species

take advantage of seed dispersal service provided by native birds?

Biological Invasions 18: 677–687.

Wang, T., A. Hamann, D. Spittlehouse, and C. Carroll. 2016. Locally

downscaled and spatially customizable climate data for historical and

future periods for North America. PLoS One 11: e0156720.

Ware, S. 2002. Rock outcrop plant communities (glades) in the Ozarks: a

synthesis. Southwestern Naturalist 47: 585–597.

Warton, D. I., R. A. Duursma, D. S. Falster, and S. Taskinen. 2012. smatr

3–an R package for estimation and inference about allometric lines.

Methods in Ecology and Evolution 3: 257–259.

Wiens, J. J. 2007. Speciation and ecology revisited: phylogenetic niche

conservatism and the origin of species. Evolution 58: 193–197.

Wiens, J. J., D. D. Ackerly, A. P. Allen, B. L. Anacker, L B. Buckley,

H. V. Cornell, E. I. Damschen, et al. 2010. Niche conservatism as an

emerging principle in ecology and conservation biology. Ecology

Letters 13: 1310–1324.

Wilczek,A.M.,L.T.Burghardt,A.R.Cobb,M.D.Cooper,S.M.Welch,and

J. Schmitt. 2010. Genetic and physiological bases for phenological

responses to current and predicted climates. Philosophical Transactions

of the Royal Society, B, Biological Sciences 365: 3129–3147.

Willis, C. G., E. R. Ellwood, R. B. Primack, C. C. Davis, K. D. Pearson,

A. S. Gallinat, J. M. Yost, et al. 2017. Old plants, new tricks:

phenological research using herbarium specimens. Trends in Ecology

& Evolution 32: 531–546.

Willis,C.G.,B.R.Ruhfel,R.B.Primack,A.J.Miller‐Rushing,

J. B. Losos, and C. C. Davis. 2010. Favorable climate change

response explains non‐native species' success in Thoreau's woods.

PLoS One 5: e8878.

Yu, H., E. Luedeling, and J. Xu. 2010. Winter and spring warming result in

delayed spring phenology on the Tibetan Plateau. Proceedings of the

National Academy of Sciences, USA 107: 22151–22156.

Yue, X., N. Unger, T. F. Keenan, X. Zhang, and C. S. Vogel. 2015. Probing

the past 30‐year phenology trend of US deciduous forests.

Biogeosciences 12: 4693–4709.

Zettlemoyer, M. A., K. Renaldi, M. D. Muzyka, and J. A. Lau 2021.

Extirpated prairie species demonstrate more variable phenological

responses to warming than extant congeners. American Journal of

Botany 108: 958–970.

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

13 of 14

Zollner,D.,M.H.MacRoberts,B.R.MacRoberts,andD.Ladd.2005.Endemic

vascular plants of the Interior Highlands, U.S.A. SIDA 21: 1781–1791.

SUPPORTING INFORMATION

Additional supporting information can be found online in

the Supporting Information section at the end of this article.

APPENDIX S1. Ancillary analyses and results for Leaven-

worthia phenology.

How to cite this article: Bartlett, Kelsey B., Matthew

W. Austin, James B. Beck, Amy E. Zanne, and Adam

B. Smith. 2023. Beyond the usual climate? Factors

determining ﬂowering and fruiting phenology across

a genus over 117 years. American Journal of Botany

e16188. https://doi.org/10.1002/ajb2.16188

14 of 14

FACTORS DETERMINING LEAVENWORTHIA PHENOLOGY

Fluctuating reproductive isolation and stable ancestry structure in a fine-scaled mosaic of hybridizing Mimulus monkeyflowers

Article

Full-text available

Mar 2025
PLOS GENET

Hybridization among taxa impacts a variety of evolutionary processes from adaptation to extinction. We seek to understand both patterns of hybridization across taxa and the evolutionary and ecological forces driving those patterns. To this end, we use whole-genome low-coverage sequencing of 458 wild-grown and 1565 offspring individuals to characterize the structure, stability, and mating dynamics of admixed populations of Mimulus guttatus and Mimulus nasutus across a decade of sampling. In three streams, admixed genomes are common and a M. nasutus organellar haplotype is fixed in M. guttatus, but new hybridization events are rare. Admixture is strongly unidirectional, but each stream has a unique distribution of ancestry proportions. In one stream, three distinct cohorts of admixed ancestry are spatially structured at ~20-50m resolution and stable across years. Mating system provides almost complete isolation of M. nasutus from both M. guttatus and admixed cohorts, and is a partial barrier between admixed and M. guttatus cohorts. Isolation due to phenology is near-complete between M. guttatus and M. nasutus. Phenological isolation is a strong barrier in some years between admixed and M. guttatus cohorts, but a much weaker barrier in other years, providing a potential bridge for gene flow. These fluctuations are associated with differences in water availability across years, supporting a role for climate in mediating the strength of reproductive isolation. Together, mating system and phenology accurately predict fluctuations in assortative mating across years, which we estimate directly using paired maternal and offspring genotypes. Climate-driven fluctuations in reproductive isolation may promote the longer-term stability of a complex mosaic of hybrid ancestry, preventing either complete isolation or complete collapse of species barriers.

Climate change increases flowering duration, driving phenological reassembly and elevated co‐flowering richness

Article

Full-text available

Jul 2024
NEW PHYTOL

Changes to flowering phenology are a key response of plants to climate change. However, we know little about how these changes alter temporal patterns of reproductive overlap (i.e. phenological reassembly). We combined long‐term field (1937–2012) and herbarium records (1850–2017) of 68 species in a flowering plant community in central North America and used a novel application of Bayesian quantile regression to estimate changes to flowering season length, altered richness and composition of co‐flowering assemblages, and whether phenological shifts exhibit seasonal trends. Across the past century, phenological shifts increased species' flowering durations by 11.5 d on average, which resulted in 94% of species experiencing greater flowering overlap at the community level. Increases to co‐flowering were particularly pronounced in autumn, driven by a greater tendency of late season species to shift the ending of flowering later and to increase flowering duration. Our results demonstrate that species‐level phenological shifts can result in considerable phenological reassembly and highlight changes to flowering duration as a prominent, yet underappreciated, effect of climate change. The emergence of an autumn co‐flowering mode emphasizes that these effects may be season‐dependent.

What Factors Determine the Natural Fruit Set of Cephalanthera longifolia and Cephalanthera rubra?

Article

Full-text available

Jun 2024
Diversity

The reproduction of rare and endangered plant species is one of the most important factors determining the stability and survival of their populations, and knowledge of the barriers to successful reproduction is essential for species conservation. Habitat loss and slow reproduction due to low fruit set are usually considered the main threats to Cephalanthera longifolia and C. rubra (Orchidaceae). The aim of this study was to analyse the natural fruit set of these species during three consecutive years in Lithuania in the northern part of the temperate zone of Europe. Six populations of C. longifolia and three populations of C. rubra were studied each year from 2021 to 2023. During the study period, 49.3% to 54.4% of C. longifolia and 40.0% to 54.3% of C. rubra individuals produced no fruit. Over the three-year period, fruit set in individual populations of C. longifolia ranged from 5.2% to 19.5%, whereas fruit set in populations of C. rubra ranged from 4.1% to 18.8%. Significant weak or moderate correlations were found between plant height, inflorescence length and the number of flowers in the inflorescence and fruit set of both species. Flower position in the inflorescence had a significant effect on fruit set in both species, and the fruit set rate of lower flowers was higher than that of upper flowers. Significant but weak correlations were found between the fruit set and most of the environmental factors analysed. The results of this study suggest that the fruit set of C. longifolia and C. rubra is dependent on insect pollination of the flowers, which in turn is affected by habitat conditions.

An Inquiry-Based Activity for Investigating the Effect of Climate Change on Phenology Using the R Programming Language

Article

Full-text available

Apr 2024
AM BIOL TEACH

Engaging students in research is increasingly recognized as a valuable pedagogical tool that can augment student learning outcomes. Here, we present an original activity that utilizes research as pedagogy to teach upper-division college students about phenological responses to climate change. By studying phenological responses in multiple species, this activity emphasizes interspecific variability in responses to a changing climate (i.e., that not all species respond in the same way), while demonstrating the relationship between environmental and phenotypic variability. In this activity, students collect data from herbarium specimens of spring ephemerals native to North America and are tasked with formulating and testing hypotheses about how the day of year that a species' flowering occurs (i.e., flowering phenology) has been affected by climate change. To accomplish this, students perform linear regressions using the R programming language-including data exploration and ensuring the dependent variable follows a normal distribution-and subsequently present their results via oral presentation. We taught this activity as a three-unit lab in an upper-division ecology course and observed quantifiable improvement in student learning outcomes. While designed as a three-unit, upper-division lab, this activity can be modified for other educational levels, blocks of time, and/or as a flipped classroom activity. Through this activity , students are provided with the opportunity to learn about the scientific method, biological collections, linear regressions, the R programming language, and scientific communication. Changes to flowering time are one of the most conspicuous effects of climate change, thus presenting an ideal topic for engaging students in biological inquiry.

The extent of introgression between incipient Clarkia species is determined by temporal environmental variation and mating system

Article

Full-text available

Mar 2024
P NATL ACAD SCI USA

Introgression is pervasive across the tree of life but varies across taxa, geography, and genomic regions. However, the factors modulating this variation and how they may be affected by global change are not well understood. Here, we used 200 genomes and a 15-y site-specific environmental dataset to investigate the effects of environmental variation and mating system divergence on the magnitude of introgression between a recently diverged outcrosser-selfer pair of annual plants in the genus Clarkia . These sister taxa diverged very recently and subsequently came into secondary sympatry where they form replicated contact zones. Consistent with observations of other outcrosser-selfer pairs, we found that introgression was asymmetric between taxa, with substantially more introgression from the selfer to the outcrosser. This asymmetry was caused by a bias in the direction of initial F1 hybrid formation and subsequent backcrossing. We also found extensive variation in the outcrosser’s admixture proportion among contact zones, which was predicted nearly entirely by interannual variance in spring precipitation. Greater fluctuations in spring precipitation resulted in higher admixture proportions, likely mediated by the effects of spring precipitation on the expression of traits that determine premating reproductive isolation. Climate-driven hybridization dynamics may be particularly affected by global change, potentially reshaping species boundaries and adaptation to novel environments.

Effects of climatic factors on strobilus production of Taurus cedar (Cedrus libani A. Rich.) populations

Article

Full-text available

Nov 2023
THEOR APPL CLIMATOL

Reproductive characteristics (e.g., pollen, strobili, cones, seeds, and fruit) are one of the main tools in sustainable forestry. However, many biotic (e.g., growth characteristics, species, population, and individual) and abiotic (e.g., edaphic, climatic, geographic, and year) factors can affect these characteristics. In this study, the impact of climatic characteristics, including minimum, maximum, and average temperatures, annual total precipitation, and relative humidity, on female and male strobilus production was examined in three natural populations of Taurus cedar (Cedrus libani A. Rich.) during three consecutive years (2020–2022). For this purpose, fifty trees were sampled randomly and marked in each population to observe strobilus production. Analysis of variance showed that climatic characteristics were similar (p > 0.05) among years and among populations, while female and male strobilus production showed significant (p < 0.01) differences among years, among populations, and among years within populations. In contrast, interactions of population × year were not significant (p > 0.05) for climatic characteristics. Two populations had the highest strobilus production (155.4 and 82.3 for females and 889.4 and 186.1 for males) in 2022. The studied climatic characteristics had no significant (p > 0.05) effects on strobilus production. The results of the study emphasized similar forestry practices in local areas based on climatic conditions.

Flowering and Fruiting Calendar of Babaçu (Attalea pindobassu): Agreement Between Local Ecological Knowledge and Phenological Monitoring in the Chapada Diamantina, Northeast Brazil

Article

Oct 2024

Babaçu (Attalea pindobassu) is a valuable palm native to the Caatinga, inhabiting the mountains of the Chapada Diamantina, northeastern Brazil. We explored the Local Ecological Knowledge (LEK) of the Coxo de Dentro extractivist community regarding babaçu’s flowering and fruiting and the alignment with the phenological pattern observed through monthly monitoring of this palm, from January to December 2021. We investigated the impact of climatic factors on the reproductive phenology of babaçu, considering LEK and monthly phenological monitoring. LEK was examined through phenological calendars developed within focus groups. The reproductive events of the babaçu were found to be continuous, with flowering responding positively to photoperiod and fruiting positively influenced by temperature, consistent with LEK of the palm’s phenology. There were no significant differences in the time intervals of reproductive events between field-monitored phenological observations and LEK. Babaçu extractivists from Coxo de Dentro possess in-depth knowledge about the reproductive phenology of this palm as well as the climatic factors affecting its phenological expression. We suggest that tapping LEK is a promising approach for rapid recognition of tropical plant phenological patterns. In the case of Attalea pindobassu, we recommend that fruit harvesting be concentrated during the fruiting peak periods of January and February.

Precipitation versus temperature as phenology controls in drylands

Article

Full-text available

Jul 2022
ECOLOGY

Cycles of plant growth, termed phenology, are tightly linked to environmental controls. The length of time spent growing, bounded by the start and end of season, is an important determinant of the global carbon, water, and energy balance. Much focus has been given to global warming and consequences for shifts in growing‐season length in temperate regions. In conjunction with warming temperatures, altered precipitation regimes are another facet of climate change that have potentially larger consequences than temperature in dryland phenology globally. We experimentally manipulated incoming precipitation in a semiarid grassland for over a decade and recorded plant phenology at the daily scale for 7 years. We found precipitation to have a strong relationship with the timing of grass greenup and senescence but temperature had only a modest effect size on grass greenup. Pre‐season drought strongly resulted in delayed grass greenup dates and shorter growing‐season lengths. Spring and summer drought corresponded with earlier grass senescence, whereas higher precipitation accumulation over these seasons corresponded with delayed grass senescence. However, extremely wet conditions diluted this effect and caused a plateaued response. Deep‐rooted woody shrubs showed few effects of variable precipitation or temperature on phenology and displayed consistent annual phenological timing compared with grasses. Whereas rising temperatures have already elicited phenological consequences and extended growing‐season length for mid and high‐latitude ecosystems, precipitation change will be the major driver of phenological change in drylands that cover 40% of the land surface with consequences for the global carbon, water, and energy balance.

Climate change is associated with increased allocation to potential outcrossing in a common mixed mating species

Article

Full-text available

Jun 2022

Premise: Although the balance between cross‐and self‐fertilization is driven by the environment, no long‐term study has documented whether anthropogenic climate change is affecting reproductive strategy allocation in species with mixed mating systems. Here, we test whether the common blue violet (Viola sororia; Violaceae) has altered relative allocation to the production of potentially outcrossing flowers as the climate has changed throughout the 20th century. Methods: Using herbarium records spanning from 1875 to 2015 from the central United States, we quantified production of obligately selfing cleistogamous (CL) flowers and potentially outcrossing chasmogamous (CH) flowers by V. sororia, coupled these records with historic temperature and precipitation data, and tested whether changes to the proportion of CL flowers correlate with temporal climate trends. Results: We find that V. sororia progressively produced lower proportions of CL flowers across the past century and in environments with lower mean annual temperature and higher total annual precipitation. We also find that both CL and CH flower phenology has advanced across this time period. Conclusions: Our results suggest that V. sororia has responded to lower temperatures and greater water availability by shifting reproductive strategy allocation away from selfing and toward potential outcrossing. This provides the first long‐term study of how climate change may affect relative allocation to potential outcrossing in species with mixed mating systems. By revealing that CL flowering is associated with low water availability and high temperature, our results suggest the production of obligately selfing flowers is favored in water limited environments.

A comparison of herbarium and citizen science phenology datasets for detecting response of flowering time to climate change in Denmark

Article

Full-text available

Mar 2022

Phenology has emerged as a key metric to measure how species respond to changes in climate. Innovative means have been developed to extend the temporal and spatial range of phenological data by obtaining data from herbarium specimens, citizen science programs, and biodiversity data repositories. These different data types have seldom been compared for their effectiveness in detecting environmental impacts on phenology. To address this, we compare three separate phenology datasets from Denmark: (i) herbarium specimen data spanning 145 years, (ii) data collected from a citizen science phenology program over a single year observing first flowering, and (iii) data derived from incidental biodiversity observations in iNaturalist over a single year. Each dataset includes flowering day of year observed for three common spring-flowering plant species: Allium ursinum (ramsons), Aesculus hippocastanum (horse chestnut), and Sambucus nigra (black elderberry). The incidental iNaturalist dataset provided the most extensive geographic coverage across Denmark and the largest sample size and recorded peak flowering in a way comparable to herbarium specimens. The directed citizen science dataset recorded much earlier flowering dates because the program objective was to report the first flowering, and so was less compared to the other two datasets. Herbarium data demonstrated the strongest effect of spring temperature on flowering in Denmark, possibly because it was the only dataset measuring temporal variation in phenology, while the other datasets measured spatial variation. Herbarium data predicted the mean flowering day of year recorded in our iNaturalist dataset for all three species. Combining herbarium data with iNaturalist data provides an even more effective method for detecting climatic effects on phenology. Phenology observations from directed and incidental citizen science initiatives will increase in value for climate change research in the coming years with the addition of data capturing the inter-annual variation in phenology.

PHENOLOGICAL SENSITIVITIES TO CLIMATE ARE SIMILAR IN TWO CLARKIA CONGENERS: INDIRECT EVIDENCE FOR FACILITATION, CONVERGENCE, NICHE CONSERVATISM, OR GENETIC CONSTRAINTS

Article

Full-text available

Dec 2021

To date, most herbarium-based studies of phenological sensitivity to climate and of climate-driven phenological shifts fall into two categories: detailed species-specific studies vs. multi-species investigations designed to explain inter-specific variation in sensitivity to climate and/or the magnitude and direction of their long-term phenological shifts. Few herbarium-based studies, however, have compared the phenological responses of closely related taxa to detect: (1) phenological divergence, which may result from selection for the avoidance of heterospecific pollen transfer or competition for pollinators, or (2) phenological similarity, which may result from phylogenetic niche conservatism, parallel or convergent adaptive evolution, or genetic constraints that prevent divergence. Here, we compare two widespread Clarkia species in California with respect to: the climates that they occupy; mean flowering date, controlling for local climate; the degree and direction of climate change to which they have been exposed over the last 115 yr; the sensitivity of flowering date to inter-annual and to long-term mean maximum spring temperature and annual precipitation across their ranges; and their phenological change over time. Specimens of C. cylindrica were sampled from sites that were chronically cooler and drier than those of C. unguiculata, although their climate envelopes broadly overlapped. Clarkia cylindrica flowers 3.5 d earlier than C. unguiculata when controlling for the effects of local climatic conditions and for quantitative variation in the phenological status of specimens. However, the congeners did not differ in their sensitivities to the climatic variables examined here; cumulative annual precipitation delayed flowering and higher spring temperatures advanced flowering. In spite of significant spring warming over the sampling period, neither species exhibited a long-term phenological shift. Precipitation and spring temperature interacted to influence flowering date: the advancing effect on flowering date of high spring temperatures was greater in dry than in mesic regions, and the delaying effect of high precipitation was greater in warm than in cool regions. The similarities between these species in their phenological sensitivity and behavior are consistent with the interpretation that facilitation by pollinators and/or shared environmental conditions generate similar patterns of selection, or that limited genetic variation in flowering time prevents evolutionary divergence between these species.

Pollination success increases with plant diversity in high‑Andean communities

Article

Full-text available

Nov 2021

Pollinator-mediated plant–plant interactions have traditionally been viewed within the competition paradigm. However, facilitation via pollinator sharing might be the rule rather than the exception in harsh environments. Moreover, plant diversity could be playing a key role in fostering pollinatormediated facilitation. Yet, the facilitative efect of plant diversity on pollination remains poorly understood, especially under natural conditions. By examining a total of 9371 stigmas of 88 species from nine high-Andean communities in NW Patagonia, we explored the prevalent sign of the relation between conspecifc pollen receipt and heterospecifc pollen diversity, and assessed whether the incidence of diferent outcomes varies with altitude and whether pollen receipt relates to plant diversity. Conspecifc pollen receipt increased with heterospecifc pollen diversity on stigmas. In all communities, species showed either positive or neutral but never negative relations between the number of heterospecifc pollen donor species and conspecifc pollen receipt. The incidence of species showing positive relations increased with altitude. Finally, stigmas collected from communities with more co-fowering species had richer heterospecifc pollen loads and higher abundance of conspecifc pollen grains. Our findings suggest that plant diversity enhances pollination success in high-Andean plant communities. This study emphasizes the importance of plant diversity in fostering indirect plant–plant facilitative interactions in alpine environments, which could promote species coexistence and biodiversity maintenance.

The evolution and systematics of Leavenworthia (Cruciferae)

Article

Jan 1963

Reed C. Rollins

Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae)

Article

Jan 1965

David G Lloyd

Region-specific phenological sensitivities and rates of climate warming generate divergent temporal shifts in flowering date across a species' range

Article

Oct 2021
AM J BOT

Premise: Forecasting how species will respond phenologically to future changes in climate is a major challenge. Many studies have focused on estimating species- and community-wide phenological sensitivities to climate to make such predictions, but sensitivities may vary within species, which could result in divergent phenological responses to climate change. Methods: We used 743 herbarium specimens of the mountain jewelflower (Streptanthus tortuosus, Brassicaceae) collected over 112 years to investigate whether individuals sampled from relatively warm vs. cool regions differ in their sensitivity to climate and whether this difference has resulted in divergent phenological shifts in response to climate warming. Results: During the past century, individuals sampled from warm regions exhibited a 20-day advancement in flowering date; individuals in cool regions showed no evidence of a shift. We evaluated two potential drivers of these divergent responses: differences between regions in (1) the degree of phenological sensitivity to climate and (2) the magnitude of climate change experienced by plants, or (3) both. Plants sampled from warm regions were more sensitive to temperature-related variables and were subjected to a greater degree of climate warming than those from cool regions; thus our results suggest that the greater temporal shift in flowering date in warm regions is driven by both of these factors. Conclusions: Our results are among the first to demonstrate that species exhibited intraspecific variation in sensitivity to climate and that this variation can contribute to divergent responses to climate change. Future studies attempting to forecast temporal shifts in phenology should consider intraspecific variation.

Extirpated prairie species demonstrate more variable phenological responses to warming than extant congeners

Article

Jun 2021

Premise: Shifting phenology in response to climate is one mechanism that can promote population persistence and geographic spread; therefore, species with limited ability to phenologically track changing environmental conditions may be more susceptible to population declines. Alternatively, apparently nonresponding species may demonstrate divergent responses to multiple environmental conditions experienced across seasons. Methods: Capitalizing on herbarium records from across the midwestern United States and on detailed botanical surveys documenting local extinctions over the past century, we investigated whether extirpated and extant taxa differ in their phenological responses to temperature and precipitation during winter and spring (during flowering and the growing season before flowering) or in the magnitude of their flowering time shift over the past century. Results: Although warmer temperatures across seasons advanced flowering, extirpated and extant species differed in the magnitude of their phenological responses to winter and spring warming. Extirpated species demonstrated inconsistent phenological responses to warmer spring temperatures, whereas extant species consistently advanced flowering in response to warmer spring temperatures. In contrast, extirpated species advanced flowering more than extant species in response to warmer winter temperatures. Greater spring precipitation tended to delay flowering for both extirpated and extant taxa. Finally, both extirpated and extant taxa delayed flowering over time. Conclusions: This study highlights the importance of understanding phenological responses to seasonal warming and indicates that extirpated species may demonstrate more variable phenological responses to temperature than extant congeners, a finding consistent with the hypothesis that appropriate phenological responses may reduce species' likelihood of extinction.

Photoperiod decelerates the advance of spring phenology of six deciduous tree species under climate warming

Article

Mar 2021
GLOBAL CHANGE BIOL

Vegetation phenology in spring has substantially advanced under climate warming, consequently shifting the seasonality of ecosystem process and altering biosphere-atmosphere feedbacks. However, whether and to what extent photoperiod (i.e., daylength) affects the phenological advancement is unclear, leading to large uncertainties in projecting future phenological changes. Here we examined the photoperiod effect on spring phenology at a regional scale using in situ observation of six deciduous tree species from the Pan European Phenological Network during 1980-2016. We disentangled the photoperiod effect from the temperature effect (i.e., forcing and chilling) by utilizing the unique topography of the northern Alps of Europe (i.e., varying daylength but uniform temperature distribution across latitudes) and examining phenological changes across latitudes. We found prominent photoperiod-induced shifts in spring leaf-out across latitudes (up to 1.7 days per latitudinal degree). Photoperiod regulates spring phenology by delaying early leaf-out and advancing late leaf-out caused by temperature variations. Based on these findings, we proposed two phenological models that consider the photoperiod effect through different mechanisms and compared them with a chilling model. We found that photoperiod regulation would slow down the advance in spring leaf-out under projected climate warming and thus mitigate the increasing frost risk in spring that deciduous forests will face in the future. Our findings identify photoperiod as a critical but understudied factor influencing spring phenology, suggesting that the responses of terrestrial ecosystem processes to climate warming are likely to be overestimated without adequately considering the photoperiod effect.

Beyond the usual climate? Factors determining flowering and fruiting phenology across a genus over 117 years

Abstract and Figures

Recommended publications

Estimating phenological sensitivity in contemporary vs. historical data sets: Effects of climate res...

Climate change is associated with increased allocation to potential outcrossing in a common mixed ma...

Region-specific phenological sensitivities and rates of climate warming generate divergent temporal...

Complex climate‐mediated effects of urbanization on plant reproductive phenology and frost risk