UC Santa Barbara
UC Santa Barbara Previously Published Works
Title
Old Plants, New Tricks: Phenological Research Using Herbarium Specimens.
Permalink
https://escholarship.org/uc/item/3j22c19z
Journal
Trends in ecology & evolution, 32(7)
ISSN
0169-5347
Authors
Willis, Charles G
Ellwood, Elizabeth R
Primack, Richard B
et al.
Publication Date
2017-07-01
DOI
10.1016/j.tree.2017.03.015
Peer reviewed
eScholarship.org Powered by the California Digital Library
University of California
Review
Old Plants, New Tricks:
Phenological Research Using
Herbarium Specimens
Charles G. Willis,
1,
*
Elizabeth R. Ellwood,
2,
*
Richard B. Primack,
3
Charles C. Davis,
1
Katelin D. Pearson,
2
Amanda S. Gallinat,
3
Jenn M. Yost,
4
Gil Nelson,
2
Susan J. Mazer,
5
Natalie L. Rossington,
5
Tim H. Sparks,
6,7
and Pamela S. Soltis
8
The timing of phenological events, such as leaf-out and flowering, strongly
influence plant success and their study is vital to understanding how plants will
respond to climate change. Phenological research, however, is often limited by
the temporal, geographic, or phylogenetic scope of available data. Hundreds of
millions of plant specimens in herbaria worldwide offer a potential solution to
this problem, especially as digitization efforts drastically improve access to
collections. Herbarium specimens represent snapshots of phenological events
and have been reliably used to characterize phenological responses to climate.
We review the current state of herbarium-based phenological research, identify
potential biases and limitations in the collection, digitization, and interpretation
of specimen data, and discuss future opportunities for phenological investi-
gations using herbarium specimens.
The Potential for Herbarium Specimens to Expand Phenological Research
Plant phenology (see Glossary) (i.e., the seasonal timing of life-history events such as flowering
and leaf-out) is a key determinant of plant success and ecosystem productivity. Furthermore,
as phenological events are often triggered by environmental cues, especially temperature, the
study of phenology is essential for predicting how species will respond to climate change. Over
the past decade, there has been a concerted effort to incorporate phenological traits, including
the onset and duration of individual phenological phases, into evolutionary ecology and climate
change biology [1–4]. Despite the importance of phenology to plant success [5–7], however,
little is known about the phenological behavior of most species [8]. In particular, the way in
which different environmental factors serve as phenological cues across the majority of species
remains a mystery [9]. This is mainly due to the difficulty of acquiring the data necessary to identify
specific environmental factors that drive phenological transitions for a given species. The collec-
tion of these data has traditionally required long-term field observations or manipulative experi-
ments that are difficult to scale up such that they capture entire regions, communities, or plant
clades [8,9]. Efforts to collect species-level phenological data, therefore, have been pursued in
only a relatively small number of species from a limited geographic distribution and often over
short timescales, resulting in a substantial gap in our understanding of phenology [8].
To address this gap, researchers have recently turned to the vast collections of plant speci-
mens in the world’s herbaria for phenological information [10–14]. Herbarium specimens can
be viewed as records of the phenological status of an individual, population, or species at a
Trends
Phenology (i.e., the timing of flowering,
leaf-out, and other recurring biological
events) is an essential component in
measuring how species have
responded and will continue to
respond to climate change.
Herbarium specimens are increasingly
being recognized and valued as a reli-
able source for estimating phenologi-
cal behavior for a diversity of plant
species.
As millions of herbarium specimens
become available online through mas-
sive digitization efforts, developing effi-
cient methods and standards for the
collection of large amounts of speci-
men-based phenological data is vital
to leveraging these data for research
purposes.
Through integration with existing phe-
nological datasets such as remote
sensing and citizen science observa-
tions, herbarium specimens offer the
potential to provide novel insights into
plant diversity and ecosystem pro-
cesses under future climate change.
1
Department of Organismic and
Evolutionary Biology and Harvard
University Herbaria, Harvard
University, Cambridge, MA 02138,
USA
2
Department of Biological Science,
Florida State University, Tallahassee,
FL 32306, USA
TREE 2248 No. of Pages 16
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy http://dx.doi.org/10.1016/j.tree.2017.03.015 1
©
TREE 2248 No. of Pages 16
given time and place (Box 1). While the phenological information provided by an individual
specimen is limited, many specimens can be used collectively to assemble a long-term picture
of the phenological behavior of a region and the species that inhabit it. Expanded phenological
information derived from large numbers of specimens can offer insight into two key ecological
phenomena: (i) long-term shifts in phenology at a given location over decades or even centuries
[10,11,15–17]; and (ii) how seasonal or interannual environmental variation cues phenological
transitions (i.e., phenological sensitivity) [14,18,19]. It is now being recognized that herbarium
specimens provide a reliable method for estimating phenological sensitivity in plants (Box 2).
Furthermore, specimens offer unique attributes that have the potential to greatly expand our
understanding of phenology. First, specimens offer a detailed history of phenological change,
with many collections dating back centuries [20], before the modern influence of climate
change [21]. Second, given their diversity in both phylogenetic and geographic sampling
[12], specimens offer the opportunity to study the evolution of phenological traits in a wide
range of lineages and biomes as well as how phenological traits may shape patterns of diversity
under future climate change.
The pace of herbarium-based phenological research has accelerated rapidly over the past
decade (Table 1) facilitated by the increasing availability of online digitized herbarium speci-
mens [21–25]. As more of these collections are digitized and climate change research con-
tinues to advance, it is now an appropriate time to evaluate the current state of herbarium-
based phenological research and discuss potential limitations, areas for improvement, and
opportunities for future research.
Historical Uses of Herbarium Specimens to Study Phenology
For hundreds of years, botanists and naturalists have collected and preserved plants as
herbarium specimens for taxonomic research, to record the flora of a region [26], to document
their economic uses [27], and as a social hobby [28]. Traditionally specimens were not collected
with the specific intent to study phenology per se. As plant collection became more widespread
among professional botanists in the 18th and 19th centuries, however, the ancillary information
recorded and retained with each specimen became more detailed and standardized, and thus
more amenable to phenological research. Most specimen labels created during the past 150
years provide information on locality, date of collection, and habitat. In addition to label data,
physical specimens are rich with information regarding plant health, morphology, and pheno-
logical status. From these data researchers can derive descriptive estimates of a species’
reproductive season (e.g., flowers in May–June) for inclusion in published floras, species
identification, and application in horticulture. The use of such data for more detailed studies
of ecological and evolutionary processes, such as phenological sensitivity to temperature, has
been limited (Table 1).
Phenology as a field of study dates to the 18th century in Europe and even earlier in Japan and
China, where observers recorded the fl owering dates of culturally significant plants such as
cherry trees [29]. Careful observations of plant phenology and its relationship to meteorological
records became common in many European countries, the USA, Japan, South Korea, and
China during the 19th century; these observations have a rich tradition in horticulture and
agriculture [30] and natural history [31] and in the past couple of decades have been used for
climate change and ecological research [32,33]. It is only relatively recently that researchers
have begun to use herbarium specimens for plant phenological research.
Modern Uses of Herbarium Specimens to Study Phenology
The recent growth in herbarium-based phenological research is arguably a product of the
growing interest in climate change and phenology around the turn of 21st century [34].
Researchers realized that herbarium specimens could potentially be used to detect and
3
Biology Department, Boston
University, Boston, MA 02215, USA
4
Biological Science Department and
Robert F. Hoover Herbarium,
California Polytechnic State University,
San Luis Obispo, CA 93407, USA
5
Department of Ecology, Evolution,
and Marine Biology, University of
California, Santa Barbara, Santa
Barbara, CA 93106, USA
6
Coventry University, Coventry CV1
5FB, UK
7
Pozna
n University of Life Sciences,
60-625 Pozna
n, Poland
8
Florida Museum of Natural History,
University of Florida, Gainesville, FL
32611, USA
*
Correspondence:
charleswillis@fas.harvard.edu
(C.G. Willis) and
eellwood@bio.fsu.edu (E.R. Ellwood).
2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
TREE 2248 No. of Pages 16
Glossary
Citizen science: the collection of
scientific data by members of the
public, often without specific
scientific training. Citizen scientists
are participants in these efforts. They
volunteer their time to assist
professional scientists in data
collection and in return gain skills
and knowledge of timely, relevant
scientific research. Citizen science is
also known, with slight variations in
interpretation, as crowdsourced
science, public participation in
scientific research, and participatory
action research.
Digitization: the process of
supplementing objects, in this case
specimens from natural history
collections, with digital data.
Digitization of natural history
collection specimens usually involves
the curation, capturing, and
processing of a digital image of the
object, transcribing the associated
label and ledger text, and
geoferencing locality information.
Digitized data can then be made
available online for researchers,
educators, policymakers, and the
public.
Herbarium specimen: preserved
plant material. A herbarium specimen
of a vascular plant is typically created
with a representative plant sample
that is pressed, dried, mounted on
archival paper, labeled, and stored in
a herbarium. Some vascular plant
organs (e.g., flowers), as well as
most nonvascular plants (e.g., marine
algae, liverworts, bryophytes), are
instead typically stored in either a
box or a jar with preserving fluid to
retain their 3D forms.
Ontology: a controlled, structured
vocabulary that describes and
formalizes relationships among
related terms. Characteristics of
relationships are defined by an
established set of hierarchical
conditions, such as X (e.g., leaf) is ‘a
part of’ another characteristic Y (e.g.,
plant), which is ‘a member of’ subset
or group Z (e.g., organism). See
Figure 3Figure I in Box 2 for an
illustration of this hierarchical
structure.
Phenology: the study of the timing
of seasonal biological events as well
as, colloquially, the events
themselves (Box 1). Plant
phenological events include leaf-out,
flowering, fruiting, and senescence.
Phenology can be determined in a
quantify long-term phenological shifts in response to climate change [10]. This, in turn, led to the
use of specimens to estimate phenological sensitivity to various environmental factors, includ-
ing temperature, day length, and precipitation (Table S1 in the supplemental information online).
To date, specimens have been used to estimate the onset of several phenophases, including
first flowering, peak flowering, leaf-out, and fruit set, as well as the duration of entire growth
phases [19,35–41]. These phenophase estimates have been used to study long-term shifts in
phenology and phenological sensitivity to interannual climate variation (Tables 1 and S1).
A literature review focused on the modern use of herbarium specimens to study phenological
responses to climate (see the supplemental information online for a full description of our
methods) reveals interesting generalities and insights. First, studies that have investigated long-
term shifts in phenology have generally found that flowering and leaf-out times have advanced,
in some cases dramatically, over the past century (median = 9.5 days, range = 0–97 days)
(Table S1; [12,13,17,19,20,42]). These long-term trends are often in agreement with studies
that have used alternative sources, such as observational data, to study phenological shifts
[43–46]. Second, for most of the studies we reviewed the onset dates of spring flowering and
leaf-out tended to be negatively associated with winter or spring temperatures (Table S1;
[4,9,16–18]); that is, plants tended to flower and leaf-out earlier in warmer years. However,
some species and regions exhibit delayed or mixed phenological responses under warmer
temperatures, potentially because they did not experience sufficient winter chilling require-
ments or because the imprint of past climate conditions has resulted in a response lag [17,47–
49]. Third, given the span of time and geographic area that specimens encompass, they almost
always capture a greater range of climatic variation experienced by a species than traditional
long-term observational data, and thus can provide a more complete estimate of phenological
shifts over time as well as phenological sensitivity to interannual or spatial variation in climate
(Box 2; [14]).
Most studies that have used herbarium specimens have focused on a single phenological
event, most commonly the date of onset for a single phenophase (Tables 1 and S1). The most
frequently studied phenophase in relation to climate change is flowering (39 of 40 studies;
Table 1), with a specific focus on either mean flowering date or peak flowering date (Table S1).
Only a handful of studies have attempted to quantify different events within a phenophase, such
as the onset, peak, and end of flowering date [37,50,51]. Thus, the opportunities for expanded
application of comparable and new techniques are abundant. For example, specimens can be
used to assess multiple phenological characters at different stages of development (flower
buds, open flowers, old flowers, young fruits, and mature fruits), allowing researchers to
estimate the sensitivity of different points in a given phenophase as well as determine how
different phenophases are related [52]. Additionally, most herbarium-based studies have been
limited to northern, temperate biomes (Table 1 and Figure 1), mirroring geographic biases in
long-term observational data [8]. The potential to expand phenological investigation into non-
temperate biomes using specimens, however, is considerable, as illustrated by the density of
tropical and subtropical specimen records in the Integrated Digitized Biocollections (iDigBio)
database alone (Figure 1).
Several recent studies have validated herbarium phenological estimates by comparing them
with independent estimates of similar phenological phenomena (Table S1). Generally, com-
parisons with independent phenological data – using photographs (prints, negatives, slides,
and digital images) and
field observations show that herbarium-based estimates of both
phenological timing [13,25,41,53] and phenological sensitivity to climate are reliable (Box 2). At
a broader scale, additional validation of herbarium-based phenological data has come from
comparisons with satellite observations of ‘green up’ [17,18,25]. While these studies provide
important validation of herbarium-based phenological data, they are nonetheless limited in their
Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy 3
TREE 2248 No. of Pages 16
phylogenetic scope and number of regional comparisons. As the use of herbarium-based
phenological data grows, so too should efforts to independently validate these data.
Potential Limitations, Errors, and Biases in Herbarium Datasets
Herbarium-based data, like all sources of data, are subject to potential biases and limitations of
which researchers must be aware [12,54] (B.H. Daru, unpublished). Such limitations are
present from the specimen collection phase, to the digitization and processing of specimens,
to the analysis and interpretation of specimen data. By understanding and addressing these
challenges, researchers can make full and appropriate use of specimens for phenological
research.
Some limitations of using herbarium data for phenology are common to other observational
datasets and originate at the time of specimen collection, including accurate species identifi-
cation and phenological event and phase discrimination. While specimens are often correctly
identified by experienced botanists, they may still be misidentified or labeled according to
outdated taxonomy. Unlike with observational datasets, however, species and phenophase
identifications for herbarium data can easily be confirmed by revisiting anomalous specimens.
Biases Unique to Herbarium Specimens
Herbarium data are known to contain additional, unique biases that stem from the opportunistic
nature of their collection. Botanists often collect samples depending on their interests, sched-
ule, and location (e.g., near roadsides, populated areas, or universities) and not to capture the
phenological status of the plant per se (B.H. Daru, unpublished) [55]. Collection biases relating
to plant habit, morphology, and nativity may also occur in herbarium datasets; for example,
Schmidt-Lebuhn et al. [56] discovered strong biases against very small plants, plants with
brown or green inflorescences, and introduced species in a sample of Australian Asteraceae.
Rich and Woodruff [57] noted that collections are biased towards common, showy plants that
grow in clumps. Additionally, broader taxonomic, spatial, and temporal biases have been
identified with Global Biodiversity Information Facility occurrence records, which include
herbarium records [54] (B.H. Daru, unpublished).
Specific to phenology, plants may be less likely to be collected at the very beginning or end of a
reproductive season, especially if a species is difficult to identify during these stages or is
inconspicuous. For example, Davis et al. [14] found that first-flowering date estimates from
specimens were, on average, 3 days later than first-flowering date estimates from field obser-
vations. Botanists may also collect only those individuals exhibiting a certain phenological stage
(e.g., mature flowers, fruits) to facilitate identification. However, it is also true that botanists may
deliberately collect plants that are flowering or fruiting out of season and are therefore not
representative of the overall phenology of the species. Another source of collection bias is the
tendency for large numbers of specimens to be collected during single collecting trips, which
can result in oversampling and the generation of duplicate specimens distributed to multiple
institutions that are subsequently treated as independent samples. Duplication of records is a
well-known problem, however, and efforts are currently underway to better account for
duplicate records across databases and data portals [58]. Finally, herbarium specimens often
represent only a fragment of an entire plant (for woody perennials especially), which makes it
important to consider how accurately specimens represent the phenology of the whole plant or
local population from which they are sampled.
Biases Due to Digitization
Data quality issues in herbarium data may also arise after collection, during label transcription,
or due to digitization. For example, ambiguous handwriting or descriptions can lead to the
incorrect transcription of a specimen’s location or collection date. In addition to transcription
binomial context as having occurred
or not (e.g., this plant is, or is not, in
flower). It can also be described on
an ordinal scale that starts at early
and progresses through peak, late,
and completed or with numeric
equivalents of these (i.e., 0–10 for
not yet flowering through to
completed). Many of these events
are evident on herbarium specimens.
4 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy
