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During the last centuries, humans have transformed global ecosystems. With their temporal dimension, herbaria provide the otherwise scarce long‐term data crucial for tracking ecological and evolutionary changes over this period of intense global change. The sheer size of herbaria, together with their increasing digitization and the possibility of sequencing DNA from the preserved plant material, makes them invaluable resources for understanding ecological and evolutionary species’ responses to global environmental change. Following the chronology of global change, we highlight how herbaria can inform about long‐term effects on plants of at least four of the main drivers of global change: pollution, habitat change, climate change and invasive species. We summarize how herbarium specimens so far have been used in global change research, discuss future opportunities and challenges posed by the nature of these data, and advocate for an intensified use of these ‘windows into the past’ for global change research and beyond.
Research review
Using herbaria to study global environmental change
Authors for correspondence:
Oliver Bossdorf
Tel: +49 7071 29 78809
an A. Burbano
Tel: +49 7071 601 1414
Received: 13 June 2018
Accepted: 19 July 2018
Patricia L. M. Lang
, Franziska M. Willems
, J. F. Scheepens
Hernan A. Burbano
and Oliver Bossdorf
Research Group for Ancient Genomics and Evolution, Max Planck Institute for Developmental Biology, 72076 Tubingen, Germany;
Plant Evolutionary Ecology, Institute of Evolution and Ecology, University of Tubingen, 72076 Tubingen, Germany
New Phytologist (2018)
doi: 10.1111/nph.15401
Key words: ancient DNA, biological invasions,
climate change, habitat change, herbarium,
phenology, pollution.
During the last centuries, humans have transformed global ecosystems. With their temporal
dimension,herbaria providethe otherwise scarce long-termdata crucial for tracking ecological and
evolutionary changesover this period of intenseglobal change. The sheersize of herbaria, together
with their increasing digitization and the possibility of sequencing DNA from the preserved plant
material, makes them invaluable resources for understanding ecological and evolutionary species’
responses to global environmental change. Following the chronology of global change, we
highlight how herbaria can inform about long-term effects on plants of at least four of the main
drivers of global change: pollution, habitat change, climate change and invasive species. We
summarize how herbarium specimens so far have been used in global change research, discuss
future opportunities and challenges posed by the nature of these data, and advocate for an
intensified use of these ‘windows into the past’ for global change research and beyond.
Global environmental change is one of the major challenges of the
and 21
centuries. It has been evident since the age of
industrialization in the late 18
century sometimes also referred
to as the advent of the anthropocene and has continuously gained
momentum (Fig. 1a; Steffen et al., 2011; Hamilton, 2016).
Biologists study global change for its broad ecological impact,
and its negative effects on biodiversity. Also, as it represents an
unplanned, long-term and large-scale experiment, studying global
change can promote understanding of fundamental processes such
as rapid adaptation. Experimental approaches to study these topics
are usually locally focused, and limited to a duration of a few
decades (Leuzinger et al., 2011). Although observational methods
are often more large-scale and long-term, they are with few
exceptions still restricted to a time frame of 5080 yr (Fig. 1a; Fitter
& Fitter, 2002; Thomas et al., 2004). To understand both the
extent of global change as a long-term process, and its full ecological
and evolutionary impact, global data that go back to the onset of
industrialization are crucial.
In this context, natural history collections are an underused
treasure of temporally and geographically broad samples that we
have just begun to dust off (Holmes et al., 2016). Especially rich is
the botany section of this vault: plants collected, pressed and
preserved, in most cases together with meta-information on spec ies,
collection site, date and collector (Fig. 2): In terms of extent, there
are >350 million specimens in almost 3000 herbaria world-wide
(Fig. 1b; Thiers, 2017;,
sampled from the 16
century up to today (Sprague & Nelmes,
1931), and the collections’ potential uses range from classical
taxonomy and systematics, to archaeobotany, archaeoecology and
climate change research (Funk, 2003). Because plants are sessile,
they are particularly exposed to environmental change. The time
courses of many of their responses to environmental change are
preserved in herbarium specimens, which therefore provide unique
spatiotemporal data for studying global change (Primack & Miller-
Rushing, 2009; Lavoie, 2013; Vellend et al., 2013; Meineke et al.,
Recent studies have emphasized the scientific value of herbaria
for a broad range of global change-related topics (Fig. 2; e.g. Zschau
et al., 2003; Miller-Rushing et al., 2006; Feeley & Silman, 2011;
Willis et al., 2017). Dense time-series of herbarium specimens even
permit studying long-term processes such as recent invasions and
their genetic population history (Exposito-Alonso et al., 2018a).
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Even though herbaria were used as early as in the 1960s to study
global change (e.g. Ruhling & Tyler, 1968, 1969), and are in the
process of being made available online via digitization (>46 700 000
specimens in the Integrated Digitized Biocollections portal alone; as
of 18 July 2018 (search terms: type
of record PreservedSpecimen, kingdom Plantae)), the commu-
nity has not fully adopted herbaria as valuable ‘time machines’ to the
past (Lavoie, 2013; Meineke et al.,2018).Especiallywiththeadvent
1800 1850 1900 1950 2000 2050
Largest herbaria
1. Muséum National d’Histoire Naturelle, Paris, France
2. The NY Botanical Garden, Bronx, USA
3. Royal Botanic Gardens, Kew, UK
4. Missouri Botanical Garden, St. Louis MA, USA
5. Conservatoire et Jardin botaniques, Geneva, Switzerland
6. Komarov Botanical Institute of RAS, St. Petersburg, Russia
7. Naturhistorisches Museum Wien, Vienna, Austria
8. The Natural History Museum, London, UK
9. Smithsonian Institution, Washington D.C., USA
10. Harvard University, Cambridge MA, USA
Continent Herbaria
Africa 203
Asia 794
Australia 78
Europe 1479
N America 939
S America 490
c. 9022 000
c. 53 970 000
c. 10 478 000
c. 201 149 000
c. 88 314 000
c. 26 167 000
erbaria specimens (c. 100-200+ yr)
Observational studies (c. 30-50 yr)
Experiments (few to 10-20 yr)
ine Temperature
°C vs 1960–1990 average
Parts per million (ppm)
Fig. 1 Herbaria as global change witnesses. (a) Timeline of global change, with lines tracking changes in world population, air temperature and atmospheric
during the last c. 200 years. Dashed line ends indicate future projections. Bars below plot indicate the typical temporal extent of herbarium samples vs
observational studies and experiments. (Population growth: United Nations, Department of Economic and Social Affairs, Population Division (2017); World
Population Prospects: The 2017 Revision.; temperature: representative concentration pathway 8.5, Intergovernmental
Panel on Climate Change,; (Marcott et al., 2013); CO
: (Neftel et al., 1994)). (b) Map with global distribution of herbaria (for visual clarity
displaying only herbaria of >100 000 specimens), names of the largest 10 herbaria, and number of herbaria and herbarium specimens curated per continent
(reflecting places of storage of specimens, not their origins; Herbarium data from Index Herbariorum,
Accessed in April 2018).
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of high-throughput methods and recent technical developments in
image analysis, the value of these collections is now more apparent
than ever (Munson & Long, 2017).
Simultaneously, next generation sequencing (NGS) techniques
now allow for in-depth genetic analysis of century-old specimens
up to whole genome sequencing of plants and even of their equally
preserved pathogens (e.g. Martin et al., 2013; Yoshida et al.,2013;
Durvasula et al., 2017; Exposito-Alonso et al., 2018a). This extends
the spectrum of available long-term data far beyond morphology or
phenology. For instance, dense sampling of such full genetic
information across time and geography enables population
genetics studies, to follow speciation processes through time, or to
quantify changes in genetic diversity in historical contexts. Working
with these small samples of degraded DNA so-called ancient DNA
(aDNA) retrieved from historic collections is technically challeng-
ing and has recently boomed in the animal field (e.g. Shapiro &
Hofreiter,2014; Orlando et al.,2015; Marciniak & Perry, 2017), yet
in the plant field it is still rarely used (Gutaker & Burbano, 2017).
Here, we present an overview of the different types of
herbaria analyses possible in global change research (Fig. 2).
Following a timeline from industrialization onwards, we divide
herbarium-related approaches into four main areas related to four
main drivers of global change: industrialization causing increased
pollution, which coincides with increasing loss of habitat and
changes in land use as well as climate change, and finally global
trade and transport resulting in an increasing number of invasive
species world-wide. In addition, in excursions dedicated to
molecular methods (Box 1), collection biases (Box 2) and the
digitization challenge (Box 3), we provide insight into three key
methodological issues that herbaria research is currently dealing
with, and hopefully inspire with ideas for extended utilization of
botanical collections. Our aim is to advocate broader use of herbaria
as ‘witnesses’ of global change. We believe that they have the
potential to fast-forward our understanding of the impacts of this
unplanned biological experiment, to substantiate our predictions
of its long-term outcomes, and to inform conservation measures.
Technological developments and the mechanization of work in the
second half of the 18
century, known as industrialization, changed
the landscape world-wide. Key contributors were improved efficiency
Biotic interactions
Pollution Habitat
Date of a contamination?
Relative abundances?
Species diversity?
Extinction events + causes?
Pollinator loss?
Within-species genetic
Adaptive potential?
Causes and dynamics of invasions?
Anthropogenic / historic factors?
Spatial escape upwards / polewards?
Temporal escape?
(leaf-out, flowering, fruiting)
Mismatched interactions?
(pollinator / herbivore traces)
Co-evolutionary host–pathogen dynamics?
Spread dynamics?
Causal strains?
Genetic paradox of invasions?
Genetic setups through time?
Contamination adaptation / plasticity?
Past CO2 concentrations?
(stomatal densities)
Contamination levels?
Photorespiration vs photosynthesis?
element ratios
isotope ratios
Fig. 2 Diversity of herbarium data and their
applications. Herbarium sheet in the centre
surrounded by types of data that can be
obtained from a specimen, with the questions
that these data can help to answer around,
ordered by respective global change driver.
Symbols indicate the type of data used to
address each question.
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of steam engines, the replacement of biofuels with coal and the
emergence of a chemical industry. A larger average income, increasing
population sizes and accelerated urbanization led to the production of
previously unseen quantities of waste and exhausts (Fig. 1a). Herbar-
ium specimens can be used to track historical pollution levels, to serve
as a baseline for pre-pollution conditions, and to connect waste
production with species’ reactions even at the genetic level in the
context of local adaptation, or to study long-term effects of singular
events such as the Chernobyl nuclear disaster (Heinrich et al. 1994).
Heavy metals
Metals from the atmosphere, soils and groundwater are deposited
on or taken up by plants, and remain present in herbarium
specimens, so the latter can be used as indicators of pollution, and
due to their meta-information facilitate the dating of contamina-
tion (Lee & Tallis, 1973; Shotbolt et al., 2007; Rudin et al., 2017).
Depending on species, their morphology, physiology and proxim-
ity to a pollution source, plants are exposed to and take up more or
less pollutants (Lawrey & Hale, 1981; Rudin et al., 2017).
Studying lead pollution levels, for example, the isotopic lead
composition in moss or lichen samples collected at roadsides
reflects fluctuations in local motor vehicle traffic, efforts to reduce
lead emissions and changes in petrol origin or composition over
time (Farmer et al., 2002). In addition to lead, herbarium samples
also track concentrations of other metals such as cadmium, copper
and zinc to follow their temporal and spatial trends in relation to
anthropogenic activities (Zschau et al., 2003; Shotbolt et al., 2007;
Box 1 Molecular analyses and degradation
The age of herbarium specimens is both their strength and their weakness, as aging is a corrosive process. For most chemicals, the extent, rate and end-
results of this process are not defined in herbarium samples. Still, it is clear that age, but also preservation practices or storage conditions can alter tissue
chemical contents. This is evident, for example, when N concentrations measured in stored tissues diverge from the results of previous methods and
studies in this case likely due to post-collection contamination (Nielsen et al., 2017). Hence, in-depth analyses of correlations between the age and
chemical compound quantities in old samples are necessary in order to make claims about historical absolute abundance values (Nielsen et al., 2017).
For DNA from historical samples aDNA age-related degradation dynamics are fairly well-characterized (Allentoft et al., 2012; Weiß et al., 2016).
Due to chemical modifications, DNA in dead tissue gets increasingly fragmented over time (Fig. B1a), and particularly in fragment ends, aDNA-
characteristic deamination drives nucleotide-substitutions of cytosine with thymine ((Weiß et al., 2016); Fig. B1b). This per se does not lessen the
potential of aDNA-studies (Gutaker & Burbano, 2017): specialized protocols even allow extraction of ultra-short fragments of <50 bp (Gutaker et al.,
2017), and the correlation of nucleotide misincorporations with time enables its use as authenticity criterion of ancient DNA (Sawyer et al., 2012; Weiß
et al., 2016). Still, these particular characteristics call for categorical rulesfor herbarium genetics to minimize contamination risks, verify authenticity and
maximize the information gained from precious old plants: samples have to be processed in clean room facilities to avoid contaminations with fresh
DNA, and sequenced to a certain depth to yield useful information.Pure PCR analyses on the contrary are inappropriate for aDNA studies, as they do not
allow the necessary authenticity verification and, due to the fragmentation of aDNA, are unlikely to yield consistent results.
Such quality requirements are particularly important due to the limitation of available material. Unlike traditional approaches that rely on metadata or
morphology of historical samples, molecular analyses require tissue probes and hence destructive sampling of specimens. Therefore, it is the duty of any
molecular herbarium scientist to optimize their methods, minimize the amount of sample needed, and employ state-of-the-art analyses to retrieve
maximum information from their samples. In the same vein, molecular herbarium scientists and curators should aim to maximize the detail of meta-
information that can be gathered from samples. Knowledge, for example, about temporary field collection in alcohol, or post-collection specimen
treatments with heavy metals (as insecticides or fungicides) is indispensable to assess the suitability of specimens for molecular approaches.
Furthermore, both curators and researchers need to assess specimen-label and specimen-sample pairs for their correctness, and remain cautious
particularly regarding the interpretation of trends in (molecular) data observed only in few or single samples.
Fig. B1 Typical molecular characteristics of herbarium DNA. (a) Fragment size distribution and (b) damage pattern found in ancient DNA (sample data
from Weiß et al. (2016), publicly available at ENA ID ERR964451).
050100 5 10152025150 200
20 000
10 000
Fragment length (bp) Nucleotide position in fragment (bp)
Read counts
Nucleotide substitutions (%)
C-to-T (aDNA authenticity signal)
(a) (b)
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Rudin et al., 2017). Combining pollution records and genetic
information from historical and contemporary samples from
contaminated sites can even enable studies of plants’ adaptation to
pollution at the genetic, heritable level, for example by studying the
association between pollution levels and specific alleles, and thus
give indications about long-term adaptation to changing condi-
tions. Such approaches are already well-established for contempo-
rary data alone (Kawecki & Ebert, 2004; Turner et al., 2010;
Arnold et al., 2016).
Anthropogenic nitrogen
Similarly, herbaria document human influences on global nitrogen
(N) cycling, that started with the rise of the chemical industry and
the production of fertilizers, and has peaked since c. 1960
(Millennium Ecosystem Assessment, 2005). Moss leaf N-contents
(as well as concentrations of phosphate and sulfur) determined
from stable isotope ratios enable inferences about realized N sources
and further cycling processes (Pe~nuelas & Filella, 2001). Such
analyses show a retention of additional, anthropogenic N within
terrestrial ecosystems (Pe~nuelas & Filella, 2001). Improved
knowledge of these nutrient dynamics within different ecosystems
helps us to understand eutrophication. Additional detail on the
biotic effects of N fluctuations could be retrieved via shotgun-
sequencing of historical plant roots, given that bona fide micro-
biomes could be recovered, as it has been shown that the bacterial
species composition of roots (and soils) is heavily influenced by
overabundance of N (Dynarski & Houlton, 2018).
Increased carbon dioxide
Pollutants such as N or carbon dioxide (CO
) can influence overall
organismal morphology, making their effects partially measurable
without destructive sampling. Increased fossil fuel combustion and
the concurrent increase in CO
concentrations since the industrial
revolution, for example, correlate with a reduction of stomatal
densities on the leaves of herbarium specimens. This trend was
already observed in 1987 in a 200-yr spanning study of woody
angiosperm herbaria samples. Further analyses under controlled
experimental conditions (Woodward, 1987; Pe~nuelas & Mata-
mala, 1990) confirm historic samples as proxies to reconstruct past
In addition to morphological studies, herbarium specimens
enable complementary measurement of global change effects on
plant carbon metabolism. Using mass spectrometry to estimate the
relative abundances of different carbon isotopes, studies indicate
increased water-use efficiency the ratio of photosynthesis to water
loss with rising CO
concentrations (Pe~nuelas & Azcon-Bieto,
1992; Pedicino et al., 2002). With time-series of genetic variation
from herbaria, it is now further possible to determine what part
long-term adaptive changes or phenotypic plasticity play in such
physiological or chemical responses.
There is, however, one caveat for measurements of any type of
chemical compounds in long-term stored historical samples: Do
chemicals suffer degradation processes similar to hydrolytic
damages occurring in DNA over time (see Box 1)? If so, to which
extent and at what rate do compounds degrade, and what influence
do factors like species, specimen mounting or general storage
conditions have on such a decay? Systematic studies of chemical
degradation through time will permit the assessment of whether
absolute or relative values should be used in historical specimens-
based long-term comparisons.
Habitat loss and land-use changes
Apart from pollution, increasing human population densities,
urbanization and, in particular, modern agriculture have caused
extensive losses, fragmentation or changes of natural habitats. This
Box 2 Collection biases
Imbalanced sampling is a well-acknowledged issue forthe use of herbaria, for example, to map species distributions or assess diversity (e.g. Meyer et al.,
2016; Daru et al., 2018). Temporal biases are caused by intense collection periods, and seasonal preferences (Holmes et al., 2016). Also, collections
often concentrate on easily accessible or much-frequented sites (geographic bias; e.g. Sofaer & Jarnevich, 2017), and on common or particularly
interesting species which depending on the collectors can change over time (taxonomic bias; e.g. Feeley, 2012). When working with herbarium data,
it is necessary to explicitly test for these biases, for example to avoid a few dominant species generating trends in a dataset (J
acome et al., 2007).
Depending on the type of question or analysis, biases may need to be corrected for by different means: normalizing collection efforts with different types
of reference sets (e.g. Heden
as et al., 2002; Law & Salick, 2005; Case et al., 2007), measuring invader distributions in relation to native species (Delisle
et al., 2003), or verifying trends with additional, nonherbarium datasets (e.g. Lienert et al., 2002; Kouwenberg et al., 2003; or even those from citizen
science, Spellman & Mulder, 2016). In particular when models are based on historical records, comparisons with modern data can support
extrapolations or generalizations, but only if biases have been dealt with: models, for example, in the context of invader dynamics and spread, have to
take species persistence into account, because historic occurrence does not equal contemporary presence and may cause overestimation of plants’
distribution and abundance (Pergl et al., 2012). This is particularly the case for species targeted by eradication measures, such as the human health
hazard Heracleum mantegazzianum, where herbarium specimens can indicate suitable habitats, but not current occurrence or general invasion
dynamics (Pergl et al., 2012). Furthermore, there are often no data on early invasion stages, because herbarium records indicate only the presence of a
species, whereas its absence is not reliably documented by a lack of records. Conclusions based on modeling and statistical analysis, particularly of early
invasion stages, should hence be used as indications rather than be over-relied upon (Hyndman et al., 2015). Finally, the currently rising bias of low
collection effort is a well-known problem for tropical areas (Feeley & Silman, 2011), yet is threatening to become global, via overall declining collections
(Prather et al., 2004). Although this particularly jeopardizes studies of new or recent invasions (Lavoie et al., 2012), it strongly affects all herbarium-
based research.
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affects plants’ geographic distribution and densities, for example
causing range reductions to more pristine environments
(Hallingback, 1992). Information about such habitat alterations
in response to global change are documented in herbaria.
Herbarium sheets normally contain information about the
presented species and sometimes other, associated species (referred
to in accompanying meta-information, or co-sampled with the
focal species, e.g. pathogens). Importantly, herbarium sheets also
state the time and place of collection. Hence, comparison between
past and present localities serves to infer a species’ distribution
through time (Hallingback, 1992).
Distribution changes
Many factors have contributed to converting the landscape into
a patchwork of agricultural fields, interspersed with cities and
roads: industrialization-associated population growth, urbaniza-
tion, increasing agricultural acreages due to mechanization of
work, or expansion of railroads and other transport systems.
Overall, species abundances tend to decrease with habitat and
land-use changes, as is the case, for example, for American
ginseng (Panax quinquefolius), both as a result of deforestation
and of heavy harvesting of wild populations (Case et al., 2007).
In light of an area’s geography, such data also can inform
species’ conservation and future trends (Case et al., 2007).
However, retrospective studies of species’ abundance in a certain
location based on historical collections are sensitive both to the
quality of available georeferencing data, and to fluctuating
collection efforts and other biases (see Box 2). A reference set of
specimens picked from the herbarium randomly and indepen-
dent of species identity can be used to establish a general
‘expected collecting frequency’, which can balance these biases
(e.g. Hedenas et al., 2002).
When herbarium records are used to relocate historical popu-
lations, current data complement herbarium-inferred distributions
and abundances (Lienert et al., 2002; Stehlik et al., 2007). Herbaria
may in some cases be the only documentation of (likely) extinct
species (Chomicki & Renner, 2015). Revisiting surveys can detect
such local extinction events, and, in correlation with current land-
use practices or site protection status, be used to study their causes
(Lienert et al., 2002). They can further document changes in overall
plant diversity, which, too, is affected by habitat fragmentation
(Stehlik et al., 2007). Such approaches are particularly useful to
evaluate changes in the local flora and motivate biodiversity
monitoring campaigns, and can inform large-scale diversity
surveys, as well as modeling-based inferences or predictions.
Indirect effects of habitat fragmentation
Similar to farming-related landscape changes, urbanization is a
prominent driver of biotic interaction changes. One of the most
crucial, commercially important types of plantanimal interaction
jeopardized, among others, by urbanization and diversity loss, is
pollination. Depending on a plant’s anatomy, herbaria also house
documentation of such interactions, and can illustrate pollinator
species decrease or loss. Presence or absence of pollinaria in
herbarium specimens of the orchid Pterygodium catholicum, for
example, reflects the historical pollination rate that depends strictly
on a specific bee (Rediviva peringueyi) (Pauw & Hawkins, 2011).
The bee’s decrease following urbanization is consistent with a shift
in local orchid communities towards selfing species (Pauw &
Hawkins, 2011). Impairment of interactions between plants and
their pollinators, caused for instance by such abundance decreases
or temporal mismatches, likely also leaves genetic signatures. Given
that affected biotic interactions could be identified using historical
plant and insect collections, these signatures could be traced
Box 3 Digitization challenge
Large-scale digitization is crucial to make biodiversity data more accessible, balance the unequal distribution of collections world-wide (Drew et al.,
2017; see also locations of all herbaria with >100 000 specimens world-wide, Fig. 1b), increase the use of herbaria in general, the number of specimens
included per study specifically (Lavoie, 2013), and fuel novel research (see Soltis, 2017; Soltis et al., 2018). Various online databases already offer access
to vast amounts of data (e.g.,,, but the digitization task is
enormous with over 350 million specimens to process and expensive. To optimize and speed up the process, various larger and smaller institutions
have developed affordable digitization workflows (Haston et al., 2012; Nelson et al., 2015; Thiers et al., 2016; Harris & Marsico, 2017). Depending on
data needs, digitization could be done in a prioritized way. In conservation biology, for instance, a fraction of available specimens appears to be enough
to reliably detect threatened species and trigger conservation efforts (Rivers et al., 2011). How and towards which end such prioritization is carried out,
and how large-scale digitization projects would be funded, is a question that needs to be addressed.
Apart from cost and speed, the transcription of meta-information, and particularly georeferencing information, is another digitization bottleneck.
Optical character recognition may help sorting entries by collector or country (Drinkwater et al., 2014), as might the development of semi-automated
imaging pipelines (Tegelberg et al., 2014). Other projects use citizen science approaches to transcribe specimenlabels ((Hill et al., 2012); https://www., and computer vision or machine learning (re-)classify specimens that are unidentified, or whose
identification was based on an old taxonomy (Unger et al., 2016; Carranza-Rojas et al., 2017; Gehan & Kellogg, 2017). Still, imprecise or wrong
georeferencing is common in herbarium data (Yesson et al., 2007), an issue that is particularly problematic in conservation, for species distribution
assessments, or prediction approaches (Feeley & Silman, 2010). Although care with location data from herbaria is, hence, necessary, digital field
notebook apps such as ColectoR may at least help guarantee complete and correct meta-information for novel collections (Maya-Lastra, 2016).Finally,
in light of concerns about misidentification of up to 50% of tropical specimens world-wide (Goodwin et al., 2015) and the continuously evolving
taxonomy, such notebooks, together with the aforementioned computerized identification approaches and even molecular methods, as well as
rigorous and continuous manual verification of specimen identities, are crucial to ensure the value of herbaria and herbaria databases.
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through time and inform the potential of other species-pairs to
overcome future mismatches.
Besides the apparent decrease of species diversity, losses of
within-species genetic diversity are a less conspicuous consequence
of habitat loss, and are a result of shrinking and increasingly isolated
populations (Ellstrand & Elam, 1993; Young et al., 1996).
Improved high-throughput sequencing techniques and novel
molecular approaches have recently made within-species genetic
diversity as preserved in herbaria accessible (see Box 1). This
ancient genetic information extends the information on habitat loss
and decreasing relative abundances to the genetic level (Cozzolino
et al., 2007; Martin et al., 2014b), with already few specimens
giving insights into a population’s genetic background. This is
crucial knowledge for conservation measures, as genetic diversity,
especially in times of increasingly fluctuating environmental
conditions, is an indispensable resource for heritable phenotypic
variation and rapid adaptation (Huenneke, 1991; Exposito-Alonso
et al., 2018b). Reduction of genetic diversity via abrupt decimation
of a population, referred to as a bottleneck, can hamper the
population’s persistence, as selection is less efficient in small
populations, where there is more stochasticity and less standing
variation to act upon (Ellstrand & Elam, 1993; Young et al., 1996;
Hartl & Clark, 2007). Comparison of contemporary vs historical
genetic diversity can serve to prioritize the conservation of specific
populations over others, and to identify genetically diverse source
populations for potential reintroductions to balance bottlenecks
(Cozzolino et al., 2007).
Climate change
Some factors on the rise since the start of industrialization, and
potentially even before that, have less direct, but long-term effects on
ecosystems: the so-called greenhouse gases such as methane (CH
and CO
(Fig. 1). Their atmospheric increase for CO
enhanced fossil fuel burning in factories, power plants and for
transportation causes global warming and as a result climate change
(Millennium Ecosystem Assessment, 2005). Thus, in addition to the
earlier mentioned direct effects of the pollutant CO
on plant
morphology and physiology (see the ‘Pollution’ section), progressive
-related global warming influences plantlife cycles, as is observed
for instance already in shifts of plant life cycles, as is observed for
instance already in shifts of plant phenology (timing of life cycle
events such as flowering and fruiting) to earlier dates. However,
herbaria not only directly track these climate-related plant responses,
but also give insights into their ripple-effects on pollinators,
herbivores and even nutrient cycling.
Range shifts as spatial escape
One possible response of plants to global warming can be
distributional shifts when plants escape from unfavorable condi-
tions, which is traceable using herbarium time-series. Comparison
of field with herbarium data verifies predictions that with
progressive global warming, species will move both upslope and
poleward, following their original climatic niches. For instance,
historic time-series have monitored movements and consecutive
diversity shifts in California, Costa Rica and South America as a
whole (Feeley, 2012; Feeley et al., 2013; Wolf et al., 2016), and
hence can differentiate successfully moving species from those that
may not persist under continuously changing conditions (Feeley
et al., 2013).
Phenology timing
Instead of spatial movements, plants also can escape global warming
‘in time’ by shifting phenological events like flowering or fruiting
towards more favorable conditions. To track such changes in the past,
flowering timing, for example, can be approximated from collection
dates of flowering herbarium specimens. Using a combination of
contemporary flowering time observations with a herbarium spec-
imen series across >100 yr and 37 genera, Primack and colleagues
(Primack et al., 2004) were the first to connect meteorological data
with earlier flowering, which was to a great part explained by
increasing spring temperatures. This trend has been confirmed by
multiple analogous studies (e.g. Davis et al., 2015) and also broader
approaches that integrated herbarium data with phenology records
obtained from field notes and photographs to cover recent years of
herbarium record scarcity (Panchen et al., 2012).
Spatial scale and statistical power are important factors for these
types of studies. Because phenology also depends on latitude,
altitude and other environmental factors, broad sampling is
necessary to separate climate change effects from other influences.
Moreover, as phenology is partly species- or plant functional type-
specific, it is useful to study contrasting flowering seasons, native
status, pollination syndromes or growth forms (Calinger et al.,
2013). All of this is facilitated by large-scale digitization and hence
improved accessibility of specimens world-wide (Lavoie, 2013;
Box 3). Such studies, for example, showed that annual plants are
generally more responsive to climate change than perennials
(Calinger et al., 2013; Munson & Long, 2017). Compilation of
large cross-species datasets furthermore allows the search for
phylogenetic signals and thus to identify evolutionary processes
involved in shaping the observed responses (Rafferty & Nabity,
2017). Apart from interspecies or -family variation, plant responses
also vary across geographic regions. Combination of world-wide
herbaria allows to capture such responses, enabling to include
remote localities across the globe into analyses (Hart et al., 2014;
Panchen & Gorelick, 2017).
Flowering is not the only phenological event heavily influenced
by climate change that can be tracked from herbarium specimens.
Depending on a plant’s reproductive structures, seed dispersal
timing also can be evaluated. At least for the Arctic, dispersal
timing, too, seems to advance with increasing temperatures, in
correspondence with associated flowering data (Panchen &
Gorelick, 2017). Contrariwise, it was also estimated from collec-
tion meta-information (Kauserud et al., 2008) that autumnal
mushroom fruiting, especially of early fruiting species, is delayed in
Norway, possibly reflecting a prolonged growth period due to
warm autumn and winter temperatures.
Another parameter that affects entire communities and ecosys-
tem processes is the leaf-out timing of deciduous trees, as it impacts
trophic interactions as well as nutrient and water cycling (Polgar &
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New Phytologist (2018)
Phytologist Research review Review 7
Primack, 2011). Such data collected from herbarium records track
long-term leaf-out trends (Zohner & Renner, 2014) and, for
example, confirm large-scale patterns of earlier leaf-out inferred
with satellite data (Everill et al., 2014).
Mismatching biotic interactions
Naturally, these climate change-related phenomena also affect
biotic relationships beyond plants, and hence cannot be seen
only as isolated processes. Changes of their timing are likely to
affect evolutionarily synchronized relationships, and even their
breaking-up over time is, together with flowering change,
partially recorded in herbaria. Combined with entomological
museum specimens, herbaria for example document disruption
of the plantpollinator relationship between the bee Andrena
nigroaenea and the orchid Ophrys sphegodes (Robbirt et al.,
2014). In herbivory relationships, herbarium specimens can
actually directly reflect insect reactions to warming. For
example, increased traces left by the scale insect Melanaspis
tenebricosa on maple tree leaves collected in warmer years
evidence a higher insect density, perfectly in accordance with
observations in the field (Youngsteadt et al., 2015). Herbaria
can thus help overcome the lack of historical insect abundance
records and facilitate evaluation of climate change effects
beyond plants alone.
The greatest challenge of most aforementioned approaches
investigating species’ responses to pollution, and habitat and climate
change, is their inability to distinguish between plastic responses and
evolutionary adaptation (Leger, 2013; Munson & Long, 2017), and
thus whether observed differences among herbaria specimens reflect
genetic changes or just environmentally induced phenotypic changes
caused, for instance, by physiological processes (Bradshaw, 1965;
Nicotra et al., 2010). Quantitative genetics methods using herbarium
time-series could help in disentangling these two alternative
hypotheses (Gienapp et al., 2008; Tiffin & Ross-Ibarra, 2014).
Once the genetic basis of phenotypic differences is identified, local
adaptation can be further tested using traditional approaches such as
common garden experiments and reciprocal transplant studies
(Savolainen et al., 2013).
Biological invasions
Natural long-distance dispersal of plants is rare (Nathan &
Muller-Landau, 2000), but as a side effect of global change, plants
increasingly move long distances (van Kleunen et al., 2015a). This
movement massively increased with human migration waves
towards the New World in the 16
century, and further
accelerated with growing trade and faster transportation
coinciding with the core time range of herbarium collections.
Today, jet-setting plant stowaways establish as ‘neophytes’, ‘aliens’
or ‘invaders’ wherever conditions are favorable enough. With this
growing alien species richness, the global species distribution is
getting more homogenous (Winter et al., 2009). Local plants lose
habitats and thus genetic diversity to the invaders, which are
therefore considered a threat to biodiversity (Millennium Ecosys-
tem Assessment, 2005).
Understanding invasion dynamics
Understanding the causes and spatiotemporal dynamics of inva-
sions is indispensable to prevent further damage, preserve natural
ecosystems and prioritize management actions (Vilaet al., 2011;
van Kleunen et al., 2015b). Although contemporary surveys depict
the current status of invasive species, herbaria track invasions from
the first recorded colonizer onwards which can serve as a proxy,
even if it is not the actual first colonizer. In conjunction with
contemporary collections and literature surveys, herbaria are
crucial to establish inventories of introduced species that monitor
their status of naturalization or invasion and inform
management strategies (Magona et al., 2018). With native plants
as baseline for collection efforts and abundance, herbaria illustrate
geographical and temporal spreads (Crawford & Hoagland, 2009)
that may in search for invasion causes be connected with historic
events. For instance, a map of Chilean alien expansions uncovers
two spread peaks, one connected to the spread of agriculture, the
other to its increased mechanization (Fuentes et al., 2008).
Understanding such causalities can feed early preventive measures:
retrospectively mapped invasions identify geographic invasion
hotspots, and the environmental and anthropogenic factors crucial
for their creation. In this way, herbaria can contribute to
understanding the general invasibility of particular habitats (Aikio
et al., 2012; Dawson et al., 2017). Furthermore, combined with
contemporary data, they can help to identify characteristics of
successful invaders, and to quantitatively connect and established
naturalization risk with external factors, and rank potential new
invaders (Dodd et al., 2016).
Herbaria also provide a means of assessing the continued success
of invasive species after establishment in a new environment.
Previous studies have used them both to predict and to verify
predictions of the climatic niche that plants can potentially occupy.
For example, the size of the native range of an invasive species has
been found to be highly correlated with its abundance in the new
range, as documented for many highly invasive Eurasian species
around Quebec (Lavoie et al., 2013). Herbaria also can enable
estimation of a weediness index or how much a plant associates
with human-caused disturbance which often also overlaps with
plant invasiveness (Robin Hart, 1976). Such estimates hold well in
comparison with field surveys (Hanan-A et al., 2015). More precise
forecasts of a species’ spread can further include its native climate
range, again extrapolated from herbarium records, thereby roughly
visualizing occupation of a possible climatic niche (Bradley et al.,
2015). Much as surveying and modeling the dynamics and spread
of invaders is crucial to inform containment measures, it is very
sensitive to biases and errors in historical collections one crucial
and common error being misidentification and misnaming (Jacobs
et al., 2017) and increasingly at risk from decreasing collection
efforts (see Box 2).
Genetic changes of invaders
Irrespective of whether invasive species stay within their native
climatic range or move beyond, they face challenges when
establishing in new environments. Successful invasive species often
New Phytologist (2018) Ó2018 The Authors
New Phytologist Ó2018 New Phytologist Trust
Review Research review
adjust to the novel conditions, and it is therefore important to
understand such changes in the invasive range.
Adjustment of morphological traits to novel environments is
often well-captured in herbaria, as demonstrated with Australian
invasives where 70% of surveyed species showed at least one
phenotypic trait changing over time (Buswell et al., 2011). With
NGS, it is now possible to define whether this trait variation is
associated with genomic changes caused either by drift or
potentially adaptive or more likely the result of phenotypic
plasticity. In addition, these methods can potentially solve the
‘genetic paradox of invasion’: the surprising success and spread of
colonizers in spite of their reduced genetic diversity (Estoup et al.,
2016): Do these species adapt based on their (reduced) standing
genetic variation, do they borrow pre-adapted standing variation
from native species (adaptive introgression; Keller & Taylor, 2010;
Arnold et al., 2016), or do they rely on de novo mutations and hence
novel variation (Exposito-Alonso et al., 2018a)?
Comparison of historic native and invasive populations with
contemporary genetic diversity can also point to diversification or
hybridization events before species expansion. A recent herbarium
genetics study, for example, has shown strong divergences of
flowering time genes particularly during the establishment phase of
the invader Sisymbrium austriacum ssp. chrysanthum, possibly
enabling a subsequent spread (Vandepitte et al., 2014). Such
patterns change over the course of invasion. In the Eurasian Alliaria
petiolata invading North America, invasive success declines along
with population age and reduced phytotoxin production in late
stages of invasion (Lankau et al., 2009). Contrary to that, chemical
analyses of herbarium specimens of the phototoxic Pastinaca sativa,
a European weed also invading North America, displays increased
concentrations of phytochemicals over time since invasion, which
coincide with the emergence of the herbivore Depressaria
pastinacella (Zangerl & Berenbaum, 2005). Studies using ancient
DNA also have pointed to anthropogenic landscape disturbances
causing genetic admixture in Ambrosia artemisiifolia’s native
populations before its introduction to new habitats, potentially a
prerequisite for later invasive success (Martin et al., 2014b). In this
sense, herbarium material allows us to compare genetic composi-
tion through time, and to identify so-called ‘cryptic’ (i.e. hidden)
invasions, where native genotypes are dispelled by phenotypically
indistinguishable but more successful and aggressively spreading
non-native relatives (Saltonstall, 2002).
Hitchhiking invaders: pathogens and herbivores
Moving beyond plant invasions, herbaria even harbor information
about hitchhikers traveling with the original plant stowaways,
pathogens, purposely or unknowingly sampled together with their
hosts (Yoshida et al., 2014). Thereby, they track the invasion
(success) stories of plant pathogens such as Phytophthora infestans,
the microbe at the root of potato late blight and the Irish potato
famine (Martin et al., 2013, 2014a; Yoshida et al., 2013). Other
preserved pathogens of particular interest for agriculture include
rust fungi and downy-mildew-causing oomycetes. Herbaria allow
identification of causal strains, their genetic characteristics and their
tracking to contemporary pathogen diversity. Coupled with host
plant analyses, they provide a (genetic) timeline of hostpathogen
dynamics to study and illustrate co-evolutionary principles such as
the arms race between hosts and their pathogens. Genetic analysis
of such systems can hence provide crucial insight into spread
dynamics of pathogens that could have devastating consequences
on crop monocultures world-wide.
Even for invasive herbivores, historic samples may contain a
genetic record. The horse chestnut leaf-mining moth Cameraria
ohridella, for example, is preserved pressed and dried in leaves of its
host plant (Lees et al., 2011). Genetics can backtrack the moth’s
spread from its native Balkan region, and in conjunction with host
plant analyses may identify resistant cultivars and biocontrol agents
for the invasive pest (Lees et al., 2011).
Conclusions and outlook
Plants preserved in herbaria offer unique perspectives on global
change and its consequences, as they are directly affected victims
(Fig. 2). Thus, they represent an invaluable temporal, geographical
and taxonomic extension of currently available data employed to
understand global environmental change, predict its course and
inform conservation measures. To fully take advantage of this
potential, and to increase and sustain the value of herbaria for the
future, three core areas demand particular attention: the mainte-
nance and curation of herbaria including continued collection
efforts, the digitization of collections, and herbarium genomics (see
also Boxes 13).
Even though many herbaria are already investing in digitization,
only a fraction of the c. 350 million specimens world-wide have
been digitized so far. Large-scale digitization would both encourage
the use of herbaria for research, and strengthen projects (e.g.
Munson & Long, 2017), as studies including digitized material are
able to use large sample sizes (Lavoie, 2013). Fast processing of
specimens at consistently high data quality is crucial for making
digital herbaria truly useful (Yesson et al., 2007), as is substantial
funding to enable this task and secure databases’ continuity. Yet,
even with increased digitization, the actual power of herbaria for
climate change study amongst other types of research lies in their
continuity through time. Despite growing recognition of the value
of herbaria, this characteristic is currently threatened by declining
collection efforts (i.e. Prather et al., 2004; Meyer et al., 2016) and a
frequent lack of support for herbaria world-wide. Consequences of
reduced data for modeling and other analyses can already be seen in
the tropics, where collections are generally sparse (Feeley & Silman,
2011). To maintain herbaria as the treasure they are today,
continued and consistent collection world-wide is essential,
especially because they have recently revealed themselves as a
browsable repository of genetic variation and diversity. This
drastically increases the value of herbaria for climate change
research, and for understanding principles of adaptation and
evolution in this context. To date, herbaria are still underused in
this aspect (Lavoie, 2013), and in particular, high-quality
sequencing data are scarce. With firm guidelines for protocols
and quality standards, pointing also to the necessity of DNA
preservation-informed sequencing efforts, this neglect is likely to
change in the coming years.
Ó2018 The Authors
New Phytologist Ó2018 New Phytologist Trust
New Phytologist (2018)
Phytologist Research review Review 9
Hence, being aware of the answers herbaria can give if we use the
right methods to ask, it is up to us to keep herbaria alive and well,
define what we need to know, and start the questioning.
We thank Moises Exposito-Alonso, Clemens Weiß and other
members of the Research Group for Ancient Genomics and
Evolution for support and suggestions.We also thank the three
anonymous referees for their helpful comments, and apologize to
colleagues whose work could not be cited owing to space
constraints. This work was supported by the German Research
Foundation (DFG; projects BO 3241/7-1 and BU 3422/1-1) and
by the Presidential Innovation Fund of the Max Planck Society.
The authors declare no competing or financial interests.
Author contributions
O.B., H.A.B., F.M.W., P.L.M.L. and J.F.S. developed the ideas for
this review; F.M.W. and P.L.M.L. undertook the literature
research and P.L.M.L. designed the figures and wrote the paper
with input from all authors.
Oliver Bossdorf
Hernan A. Burbano
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... Molecular analyses of historical DNA from herbarium specimens can help to overcome such methodological issues, as historical collections provide unique insights into recent population histories (James et al., 2018;Lang et al., 2019). Population genetic comparisons between historical and current populations allow us to study the adverse effects of recent habitat alterations on currently threatened populations (Meinicke et al., 2018;Lang et al., 2019;Albani Rocchetti et al., 2021). ...
... Molecular analyses of historical DNA from herbarium specimens can help to overcome such methodological issues, as historical collections provide unique insights into recent population histories (James et al., 2018;Lang et al., 2019). Population genetic comparisons between historical and current populations allow us to study the adverse effects of recent habitat alterations on currently threatened populations (Meinicke et al., 2018;Lang et al., 2019;Albani Rocchetti et al., 2021). In particular, such comparisons can document the consequences of genetic drift in populations that have become smaller and increasingly isolated, which may reveal if and how much genetic diversity has been lost through space and time (Cozzolino et al., 2007). ...
... Nualart et al., 2017;Liu et al., 2020;Albani Rocchetti et al., 2021), underlining the need for future research on genetic diversity in current vs. historical samples. However, there are limitations in the use of herbaria related to collection biases (reviewed by Lang et al., 2019). Sampling efforts may differ through time (i.e. ...
Background and Aims Habitat degradation and landscape fragmentation dramatically lower population sizes of rare plant species. Decreasing population sizes may, in turn, negatively affect genetic diversity and reproductive fitness which can ultimately lead to local extinction of populations. Although such extinction vortex dynamics have been postulated in theory and modelling for decades, empirical evidence from local extinctions of plant populations is scarce. In particular, comparisons between current vs. historical genetic diversity and differentiation are lacking despite their potential to guide conservation management. Methods We studied the population genetic signatures of the local extinction of Biscutella laevigata subsp. gracilis populations in Central Germany. We used microsatellites to genotype individuals from 15 current populations, one ex-situ population, and 81 herbarium samples from five extant and 22 extinct populations. In the current populations, we recorded population size and fitness proxies, collected seeds for a germination trial and conducted a vegetation survey. The latter served as surrogate for habitat conditions to study how habitat dissimilarity affects functional connectivity among the current populations. Key Results Bayesian clustering revealed similar gene pool distribution in current and historical samples but also indicated that a distinct genetic cluster was significantly associated with extinction probability. Gene flow was affected by both spatial distance and floristic composition of population sites, highlighting the potential of floristic composition as powerful predictor of functional connectivity which may promote decision making for reintroduction measures. For an extinct population, we found a negative relationship between sampling year and heterozygosity. Inbreeding negatively affected germination. Conclusions Our study illustrates the usefulness of historical DNA to study extinction vortices in threatened species. Our novel combination of classical population genetics together with data from herbarium specimens, an ex-situ population and a germination trial underscores the need for genetic rescue measures to prevent extinction of B. laevigata in Central Germany.
... This further complicates the usage of DNA from plant herbarium tissues (Kistler, 2012;Alsos et al., 2020). Additionally, the quality and quantity of DNA found in herbarium specimens depend on the conditions to which the specimens were exposed during collection and storage, and are, in general, lower than for freshly collected, silica-dried, or frozen plant materials (Staats et al., 2011;Drábková, 2014;Lang et al., 2019). ...
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Premise: Herbaria harbor a tremendous number of plant specimens that are rarely used for molecular systematic studies, largely due to the difficulty in extracting sufficient amounts of high-quality DNA from the preserved plant material. Methods:We compared the standard Qiagen DNeasy Plant Mini Kit and a specific protocol for extracting ancient DNA (aDNA) (the N-phenacylthiazolium bromide and dithiothreitol [PTB–DTT] extraction method) from two different plant genera (Xanthium and Salix). The included herbarium materials covered about two centuries of plant collections. To analyze the success of DNA extraction using each method, a subset of samples was subjected to a standard library preparation as well as target-enrichment approaches. Results: The PTB–DTT method produced a higher DNA yield of better quality than the Qiagen kit; however, extracts from the Qiagen kit over a certain DNA yield and quality threshold produced comparable sequencing results. The sequencing resulted in high proportions of endogenous reads. We were able to successfully sequence 200-year-old samples. Discussion: This method comparison revealed that, for younger specimens, DNA extraction using a standard kit might be sufficient. For old and precious herbarium specimens, aDNA extraction methods are better suited to meet the requirements for next-generation sequencing.
... It is also clear that digitisation has been invaluable during national COVID-19 lockdowns. These initiatives have made images and associated data available to taxonomists as well as a wide range of other scientific and non-scientific researchers including ecologists, climate scientists, biogeographers, computer modelers, pollution researchers, historians and artists (e.g., Peñuelas & Filella, 2002;Funk, 2003;IUCN, 2012;Yoshida & al., 2013;DRYFLOR, 2016;Rudin & al., 2017;Lang & al., 2018, Moonlight & al., 2020Willis & al., 2020) as a source of information and inspiration. ...
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In response to the worldwide coronavirus outbreak, which effectively shut down fieldwork, laboratory and herbarium‐based studies, an evaluation was made of the effectiveness and limitations of undertaking a virtual taxonomic study using only online herbarium specimen resources related to the genus Madhuca (Sapotaceae) for the Flora of Singapore. The study demonstrated the immense value of digital images to basic taxonomic research but also found that diagnostic micro‐morphological characters, often critical in defining species boundaries, cannot be seen in many digital images, even at high resolution. Several recommendations are made on how to maximise the utility of online herbarium specimen images to help facilitate future taxonomic research, though it is clear that physical access to herbarium specimens remains essential.
... Alternative tools that use images of the specimen on the herbarium mounting sheet would greatly help botanists and taxonomists working in herbaria. There is increasing interest in the digitization of herbarium specimens (Daru et al., 2018;Davis et al., 2015;Espinosa and Pinedo Castro, 2018;Lang et al., 2019;Pearson, 2019;Wang, 2018). This is mainly due to current initiatives to digitize biodiversity data and make them accessible to a larger audience worldwide (Hedrick et al., 2020). ...
Herbaria contain the treasure of millions of specimens that have been preserved for several years for scientific studies. To increase the rate of scientific discoveries, digitization of these specimens is currently ongoing to facilitate the easy access and sharing of data to a wider scientific community. Online digital repositories such as Integrated Digitized Biocollection and the Global Biodiversity Information Facility have already accumulated millions of specimen images yet to be explored. This presents the perfect time to take advantage of the opportunity to automate the identification process and increase the rate of novel discoveries using computer vision (CV) and machine learning (ML) techniques. In this study, a systematic literature review of more than 70 peer-reviewed publications was conducted focusing on the application of computer vision and machine learning techniques to digitized herbarium specimens. The study categorizes the different techniques and applications that are commonly used for digitized herbarium specimens and highlights existing challenges together with their potential solutions. We hope this study will serve as a firm foundation for new researchers in the relevant disciplines and will also be enlightening to both computer science and ecology experts.
Natural history collections (NHCs) represent an enormous and largely untapped wealth of information on the Earth's biota, made available through GBIF as digital preserved specimen records. Precise knowledge of where the specimens were collected is paramount to rigorous ecological studies, especially in the field of species distribution modelling. Here, we present a first comprehensive analysis of georeferencing quality for all preserved specimen records served by GBIF, and illustrate the impact that coordinate uncertainty may have on predicted potential distributions. We used all GBIF preserved specimen records to analyse the availability of coordinates and associated spatial uncertainty across geography, spatial resolution, taxonomy, publishing institutions and collection time. We used three plant species across their native ranges in different parts of the world to show the impact of uncertainty on predicted potential distributions. We found that 38% of the 180+ million records provide coordinates only and 18% coordinates and uncertainty. Georeferencing quality is determined more by country of collection and publishing than by taxonomic group. Distinct georeferencing practices are more determinant than implicit characteristics and georeferencing difficulty of specimens. Availability and quality of records contrasts across world regions. Uncertainty values are not normally distributed but peak at very distinct values, which can be traced back to specific regions of the world. Uncertainty leads to a wide spectrum of range sizes when modelling species distributions, potentially affecting conclusions in biogeographical and climate change studies. In summary, the digitised fraction of the world's NHCs are far from optimal in terms of georeferencing and quality mainly depends on where the collections are hosted. A collective effort between communities around NHC institutions, ecological research and data infrastructure is needed to bring the data on a par with its importance and relevance for ecological research.
Today plants often flower earlier due to climate warming. Herbarium specimens are excellent witnesses of such long‐term changes. However, the magnitude of phenological shifts may vary geographically, and the data are often clustered. Therefore, large‐scale analyses of herbarium data are prone to pseudoreplication and geographical biases. We studied over 6000 herbarium specimens of 20 spring‐flowering forest understory herbs from Europe to understand how their phenology had changed during the last century. We estimated phenology trends with or without taking spatial autocorrelation into account. On average plants now flowered over 6 d earlier than at the beginning of the last century. These changes were strongly associated with warmer spring temperatures. Flowering time advanced 3.6 d per 1°C warming. Spatial modelling showed that, in some parts of Europe, plants flowered earlier or later than expected. Without accounting for this, the estimates of phenological shifts were biased and model fits were poor. Our study indicates that forest wildflowers in Europe strongly advanced their phenology in response to climate change. However, these phenological shifts differ geographically. This shows that it is crucial to combine the analysis of herbarium data with spatial modelling when testing for long‐term phenology trends across large spatial scales.
Significance Adaptive evolution can help species to persist and spread in new environments, but it is unclear how the rate and duration of adaptive evolution vary throughout species ranges and on the decadal timescales most relevant to managing biodiversity for the 21st century. Using herbarium records, we reconstruct 150 y of evolution in an invasive plant as it spread across North America. Flowering phenology evolves to adapt to local growing seasons throughout the range but stalls after about a century. This punctuated, convergent evolution recapitulates long-term dynamics in the fossil record, implicating limits to evolutionary rates that are not evident for the first century of spread.
Climate warming changes the phenology of many species. When interacting organisms respond differently, climate change may disrupt their interactions and affect the stability of ecosystems. Here, we used global biodiversity facility occurrence records to examine phenology trends in plants and their associated insect pollinators in Germany since the 1980s. We found strong phenological advances in plants but differences in the extent of shifts among pollinator groups. The temporal trends in plant and insect phenologies were generally associated with interannual temperature variation and thus probably driven by climate change. When examining the synchrony of species-level plant–pollinator interactions, their temporal trends differed among pollinator groups. Overall, plant–pollinator interactions become more synchronized, mainly because the phenology of plants, which historically lagged behind that of the pollinators, responded more strongly to climate change. However, if the observed trends continue, many interactions may become more asynchronous again in the future. Our study suggests that climate change affects the phenologies of both plants and insects and that it also influences the synchrony of plant–pollinator interactions.
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Understanding the status and extent of alien plants is crucial for effective management. We explore this issue using Australian Acacia species (wattles) in South Africa (a global hotspot for wattle introductions and tree invasions). The last detailed inventory of wattles in South Africa was based on data collated forty years ago. This paper aimed to determine: 1) how many Australian Acacia species have been introduced to South Africa; 2) which species are still present; and 3) the status of naturalised taxa that might be viable targets for eradication. All herbaria in South Africa with specimens of introduced Australian Acacia species were visited and locality records were compared with records from the literature, various databases, and expert knowledge. For taxa not already known to be widespread invaders, field surveys were conducted to determine whether plants are still present, and detailed surveys were undertaken of all naturalised populations. For all naturalised taxa we also sequenced one nuclear and one chloroplast gene to confirm their putative identities. We found evidence that 142 Australian Acacia species have been introduced to South Africa (approximately double the estimate from previous work), but we could confirm the current presence of only 33 species. Fifteen wattle species are invasive (13 are in category E and two in category D2 in the Unified Framework for Biological Invasions); five have naturalised (C3); and 13 are present but there was no evidence that they had produced reproductive offspring (B2 or C1). DNA barcoding provided strong support for only 23 taxa (including two species not previously recorded from South Africa), the current name ascribed was not supported for three species, and for a further three species there was no voucher specimen on GenBank against which their identity could be checked. Given the omissions and errors found during this systematic re-evaluation of historical records; it is clear that analyses of the type conducted here are crucial if the status of even well-studied groups of alien taxa is to be accurately determined.
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By following the evolution of populations that are initially genetically homogeneous, much can be learned about core biological principles. For example, it allows for detailed studies of the rate of emergence of de novo mutations and their change in frequency due to drift and selection. Unfortunately, in multicellular organisms with generation times of months or years, it is difficult to set up and carry out such experiments over many generations. An alternative is provided by “natural evolution experiments” that started from colonizations or invasions of new habitats by selfing lineages. With limited or missing gene flow from other lineages, new mutations and their effects can be easily detected. North America has been colonized in historic times by the plant Arabidopsis thaliana, and although multiple intercrossing lineages are found today, many of the individuals belong to a single lineage, HPG1. To determine in this lineage the rate of substitutions—the subset of mutations that survived natural selection and drift–, we have sequenced genomes from plants collected between 1863 and 2006. We identified 73 modern and 27 herbarium specimens that belonged to HPG1. Using the estimated substitution rate, we infer that the last common HPG1 ancestor lived in the early 17th century, when it was most likely introduced by chance from Europe. Mutations in coding regions are depleted in frequency compared to those in other portions of the genome, consistent with purifying selection. Nevertheless, a handful of mutations is found at high frequency in present-day populations. We link these to detectable phenotypic variance in traits of known ecological importance, life history and growth, which could reflect their adaptive value. Our work showcases how, by applying genomics methods to a combination of modern and historic samples from colonizing lineages, we can directly study new mutations and their potential evolutionary relevance.
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As Earth is currently experiencing dramatic climate change, it is of critical interest to understand how species will respond to it. The chance of a species withstanding climate change is likely to depend on the diversity within the species and, particularly, whether there are sub-populations that are already adapted to extreme environments. However, most predictive studies ignore that species comprise genetically diverse individuals. We have identified genetic variants in Arabidopsis thaliana that are associated with survival of an extreme drought event-a major consequence of global warming. Subsequently, we determined how these variants are distributed across the native range of the species. Genetic alleles conferring higher drought survival showed signatures of polygenic adaptation and were more frequently found in Mediterranean and Scandinavian regions. Using geo-environmental models, we predicted that Central European, but not Mediterranean, populations might lag behind in adaptation by the end of the twenty-first century. Further analyses showed that a population decline could nevertheless be compensated by natural selection acting efficiently over standing variation or by migration of adapted individuals from populations at the margins of the species' distribution. These findings highlight the importance of within-species genetic heterogeneity in facilitating an evolutionary response to a changing climate.
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Nitrogen (N) fixation by free-living bacteria is a primary N input pathway in many ecosystems and sustains global plant productivity. Uncertainty exists over the importance of N, phosphorus (P) and molybdenum (Mo) availability in controlling free-living N fixation rates. Here, we investigate the geographic occurrence and variability of nutrient constraints to free-living N fixation in the terrestrial biosphere. We compiled data from studies measuring free-living N fixation in response to N, P and Mo fertilizers. We used meta-analysis to quantitatively determine the extent to which N, P and Mo stimulate or suppress N fixation, and if environmental variables influence the degree of nutrient limitation of N fixation. Across our compiled dataset, free-living N fixation is suppressed by N fertilization and stimulated by Mo fertilization. Additionally, free-living N fixation is stimulated by P additions in tropical forests. These findings suggest that nutrient limitation is an intrinsic property of the biochemical demands of N fixation, constraining free-living N fixation in the terrestrial biosphere. These findings have implications for understanding the causes and consequences of N limitation in coupled nutrient cycles, as well as modeling and forecasting nutrient controls over carbon–climate feedbacks.
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Nonrandom collecting practices may bias conclusions drawn from analyses of herbarium records. Recent efforts to fully digitize and mobilize regional floras online offer a timely opportunity to assess commonalities and differences in herbarium sampling biases. We determined spatial, temporal, trait, phylogenetic, and collector biases in c. 5 million herbarium records, representing three of the most complete digitized floras of the world: Australia (AU), South Africa (SA), and New England, USA (NE). We identified numerous shared and unique biases among these regions. Shared biases included specimens collected close to roads and herbaria; specimens collected more frequently during biological spring and summer; specimens of threatened species collected less frequently; and specimens of close relatives collected in similar numbers. Regional differences included overrepresentation of graminoids in SA and AU and of annuals in AU; and peak collection during the 1910s in NE, 1980s in SA, and 1990s in AU. Finally, in all regions, a disproportionately large percentage of specimens were collected by very few individuals. We hypothesize that these mega-collectors, with their associated preferences and idiosyncrasies, shaped patterns of collection bias via 'founder effects'. Studies using herbarium collections should account for sampling biases, and future collecting efforts should avoid compounding these biases to the extent possible.
Understanding the status and extent of alien plants is crucial for effective management. We explore this issue using Australian Acacia species (wattles) in South Africa (a global hotspot for wattle introductions and tree invasions). The last detailed inventory of wattles in South Africa was based on data collated forty years ago. This paper aimed to determine: 1) how many Australian Acacia species have been introduced to South Africa; 2) which species are still present; and 3) the status of naturalised taxa that might be viable targets for eradication. All herbaria in South Africa with specimens of introduced Australian Acacia species were visited and locality records were compared with records from the literature, various databases, and expert knowledge. For taxa not already known to be widespread invaders, field surveys were conducted to determine whether plants are still present, and detailed surveys were undertaken of all naturalised populations. For all naturalised taxa we also sequenced one nuclear and one chloroplast gene to confirm their putative identities. We found evidence that 142 Australian Acacia species have been introduced to South Africa (approximately double the estimate from previous work), but we could confirm the current presence of only 33 species. Fifteen wattle species are invasive (13 are in category E and two in category D2 in the Unified Framework for Biological Invasions); five have naturalised (C3); and 13 are present but there was no evidence that they had produced reproductive offspring (B2 or C1). DNA barcoding provided strong support for only 23 taxa (including two species not previously recorded from South Africa), the current name ascribed was not supported for three species, and for a further three species there was no voucher specimen on GenBank against which their identity could be checked. Given the omissions and errors found during this systematic re-evaluation of historical records; it is clear that analyses of the type conducted here are crucial if the status of even well-studied groups of alien taxa is to be accurately determined.
Plant and fungal specimens in herbaria are becoming primary resources for investigating how plant phenology and geographic distributions shift with climate change, greatly expanding inferences across spatial, temporal, and phylogenetic dimensions. However, these specimens contain a wealth of additional data—including nutrients, defensive compounds, herbivore damage, disease lesions, and signatures of physiological processes—that capture ecological and evolutionary responses to the Anthropocene but which are less frequently utilized. Here, we outline the diversity of herbarium data, global change topics to which they have been applied, and new hypotheses they could inform. We find that herbarium data have been used extensively to study impacts of climate change and invasive species, but that such data are less commonly used to address other drivers of biodiversity loss, including habitat conversion, pollution, and overexploitation. In addition, we note that fungal specimens are under‐explored relative to vascular plants. To facilitate broader application of plant and fungal specimens in global change research, we consider the limitations of these data and modern sampling and statistical tools that may be applied to surmount challenges they present. Using a case study of insect herbivory, we illustrate how novel herbarium data may be employed to test hypotheses for which few data exist. With the goal of positioning herbaria as hubs for global change research, we suggest future research directions and curation priorities. This article is protected by copyright. All rights reserved.
Phytophthora infestans, the cause of potato late blight, is infamous for having triggered the Irish Great Famine in the 1840s. Until the late 1970s, P. infestans diversity outside of its Mexican center of origin was low, and one scenario held that a single strain, US-1, had dominated the global population for 150 years; this was later challenged based on DNA analysis of historical herbarium specimens. We have compared the genomes of 11 herbarium and 15 modern strains. We conclude that the 19th century epidemic was caused by a unique genotype, HERB-1, that persisted for over 50 years. HERB-1 is distinct from all examined modern strains, but it is a close relative of US-1, which replaced it outside of Mexico in the 20th century. We propose that HERB-1 and US-1 emerged from a metapopulation that was established in the early 1800s outside of the species' center of diversity.