2020 - Lagomarsino & Frost - The Central Role of Taxonomy in The Study of Neotropical Biodeiversity

THE CENTRAL ROLE OF Laura P. Lagomarsino2* and Laura A.
Frost2
TAXONOMY IN THE STUDY OF
NEOTROPICAL BIODIVERSITY1
ABSTRACT
The Neotropics are the most species-rich area of the planet. Understanding the origin and maintenance of this diversity is an
important goal of ecology and evolutionary biology. Success in this endeavor relies heavily on the past work of taxonomists who have
collected specimens and produced the floras and monographs that constitute the foundation for the study of plant diversity. To
illustrate this, we visualize collecting efforts through time and identify the importance of past taxonomic and collection efforts in
generating the bulk of specimen data that broad-scale analyses rely on today. To demonstrate the importance of taxonomy for the
study of Neotropical biodiversity, we showcase selected plant groups in which in-depth taxonomic understanding has facilitated
exciting evolutionary and ecological research and highlight the teams of scientists who have built on the legacy of Alwyn Gentry,
one of the most prolific taxonomists of the late 20th century. We also discuss challenges faced by taxonomists, including perceived
subjectivity, difficulty in measuring impact, and the need to become more interdisciplinary. We end with potential solutions going
forward, including integration of taxonomists in interdisciplinary research, advocacy for continued collection efforts, increased
funding for alpha taxonomic research that is performed with increasingly replicable methodology, and explicit decolonization
efforts to increase inclusivity and equity in the field of taxonomy. Acknowledging the central role of taxonomy and taxonomists is
essential to accurately and completely describe Neotropical biodiversity patterns in an age of unprecedented extinction risk and
conservation need.
Key words: Biodiversity, Central America, decolonialization, floristics, herbarium, monography, museum-based research,
South America, taxonomic impediment.
For centuries, scientists have tried to understand the demonstrate the importance of dispersal barriers in
distribution of life on earth and why some geographic structuring genetic diversity (Dick & Heuertz, 2008;
regions house much higher species diversity than Nazareno et al., 2017) and clade-focused phylogenetic
others. The latitudinal species diversity gradient, with studies that make a case for both biotic and abiotic
species richness being highest surrounding the equator factors in driving diversification across the Neotropics
and decreasing toward the poles (Hawkins, 2001), is a (Lagomarsino et al., 2016), shed light on the origin of
classic area of inquiry. Likewise, the high species rich- this biodiversity. On more recent time scales, commu-
ness in the Neotropics compared to other tropical regions nity ecology provides insights into the coexistence of
of the globe has inspired innumerable research programs species in diverse communities (Eck et al., 2019) and
(see Antonelli & Sanmartı́n, 2011). Understanding the the role of environmental gradients in structuring plant
origin and maintenance of this exceptional biodiversity phenotypic diversity (Umaña & Swenson, 2019), both of
is a fundamental aim of ecology and evolutionary biology which are likely tied to plant secondary chemistry
today (Antonelli et al., 2017). (Sedio, 2017) and regional attributes (Ricklefs & He,
It is not surprising that these questions have attracted 2016). These studies demonstrate how extant biodi-
researchers across subfields, many of which were versity is maintained. Paleobiology further links major
highlighted in the 66th Annual Fall Symposium of the changes in climate and landscape, such as mountain
Missouri Botanical Garden. Evolutionary studies, includ- uplift and changes in drainage systems, to shifts in
ing phylogeographic analyses of widespread taxa that biodiversity over deep geological timescales (Claramunt
1 L. P. L. would like to thank Mónica Carlsen, Sebastián Tello, and James Miller, the organizers of the 66th Annual Fall
Symposium of the Missouri Botanical Garden, for their hard work in assembling a diverse lineup of speakers, and for including her
among them. L. P. L.’s time at MO between 2015 and 2017, funded by a National Science Foundation Postdoctoral Research
Fellowship in Biology (grant no. 1523880), shaped many of the ideas presented here, especially conversations with: Tom Croat, Roy
Gereau, Michael Grayum, Iván Jimenéz, Ron Leisner, Jim Miller, Rosa Ortiz-Gentry, John Pruski, Jim Solomon, Peter Stevens,
Charlotte Taylor, Carmen Ulloa-Ulloa, Henk van der Werff, and Jim Zarucchi†. Even while these individuals may have been
influential to our thinking, they certainly may not agree with everything we have written. Lúcia Lohmann, Doug Daly, Paul Fine,
and Sandra Knapp provided invaluable comments that resulted in an appreciably better, more balanced manuscript, and, as
always, conversations and comments from Daniel Santamarı́a-Aguilar resulted in further improvements. L. P. L. and L. A. F. are
funded by a grant from the Louisiana Board of Regents Research Competitiveness Subprogram. We dedicate this manuscript to all
Neotropical plant taxonomists, past and present, who have devoted their lives to cataloging the most species-rich area of the world,
thereby providing the basis for our current understanding about the biodiversity of this incredibly diverse region.
2 Shirley C. Tucker Herbarium, Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, U.S.A.
* Author for correspondence: [email protected]
VERSION OF RECORD FIRST PUBLISHED ONLINE ON 30 SEPTEMBER 2020 AHEAD OF FALL 2020 ISSUE.
doi: 10.3417/2020601 ANN. MISSOURI BOT. GARD. 105: 405–421.
406 Annals of the
Missouri Botanical Garden
& Cracraft, 2015), and recent millennia (Pupim et al., refined understanding of relationships among organ-
2019; Åkesson et al., 2020). isms, facilitating broad comparative analyses that have
The study of Neotropical biodiversity patterns is shed light on the generalities of the evolutionary process
becoming increasingly interdisciplinary, merging tech- (Hinchliff et al., 2015; Diaz et al., 2019; One Thousand
niques from various subdisciplines (Ribas et al., 2012; Plant Transcriptomes Initiative, 2019). However, basic
Bacon et al., 2015; Salazar et al., 2018; Hoorn et al., monographic work, the foundation of all biodiversity
2019). The robust community that studies Neotropical studies (Heywood, 2001), has not kept pace, with es-
biodiversity benefits immensely from the past work of timates suggesting that this branch of study has been
taxonomists (Mori, 1992). Indeed, these professionals either in decline or in a period of relative stagnation in
are often the unsung heroes in broad studies of biodi- recent decades (Heywood, 2001; Tancoigne & Dubois,
versity. The floras and monographs that they author 2013; Bebber et al., 2014; Miralles et al., 2020). This is
and the collections they make in the field represent the despite the complementary nature of these subdisci-
primary resources for biodiversity documentation. Like- plines of systematics. Indeed, while phylogeneticists
wise, their hypotheses about species limits are tested test hypotheses formulated by taxonomists and pub-
explicitly by molecular systematists and represent the lished in monographs, taxonomists re-circumscribe taxa
basic working units used by ecologists. Furthermore, to reflect the evolutionary relationships published by
their deep understanding of specific taxa and/or re- phylogeneticists.
gional biodiversity has inspired many studies. The ability to accurately name species and to de-
Even though taxonomists provide the foundation work scribe new diversity as it is discovered is key to un-
to biodiversity science, their contributions are often derstanding broad biodiversity patterns. However, the
under-recognized. For example, even though species subset of researchers who are trained to do this is small,
identification is crucial to reproducibility (Por, 2007) and is actually shrinking as many experts head into
and determination can be incredibly time-consuming retirement without guaranteed lines to replace them
(Mori, 1992), taxonomists’ identifications are rarely (Gaston & May 1992; Buyck, 1999). This illustrates
acknowledged in publications. Likewise, the checklists, the taxonomic impediment (Cardoso et al., 2017), which
floras, and monographs that inspire so many ecological refers to the disconnect between the diminishing pool of
projects and from which data are mined for large-scale researchers who generate floristic inventories and make
studies often go uncited, devaluing the massive amount taxonomic decisions, and those who use them. Lack of
of labor necessary to compile those lists. Further, the basic taxonomic understanding has measurable conse-
botanists who collect the bulk of contemporary herbar- quences. First, it means that only a small subset of the
ium specimens see no benefit in their profile or reach biology community has the skills to identify organisms,
relative to those that do not voucher their research. especially in species-rich tropical regions, and a result-
Here, we argue that without foundational knowledge ingly small subset can describe new diversity as it is
of alpha taxonomy, the research featured in the 66th encountered (Wheeler, 2020). Second, it implies that
symposium of the Missouri Botanical Garden would not changing taxonomic concepts are curated by a relatively
have been possible. It is thus appropriate that many small number of employed taxonomists, each with a
speakers honored Alwyn Gentry’s scientific legacy. necessarily narrow realm of specialty, leading to mas-
Gentry’s hypotheses remain a cornerstone in the study sive numbers of misidentified specimens in herbaria
of Neotropical biodiversity; perhaps less widely known, (Goodwin et al., 2015). This is perhaps exacerbated by
Gentry was also one of the most prolific taxonomists of the increased reliance on specimens from plot inven-
the late 20th century (Miller et al., 1996). tories for understanding ecology of Neotropical ecosys-
tems. While these studies generate important data that
THE TAXONOMIC IMPEDIMENT AND THE IMPORTANCE OF
are directly connected to herbarium vouchers, up to
EXPERT KNOWLEDGE 50% of these specimens are thought to be erroneously
identified (Baker et al., 2017), perhaps in part because
One of the most important goals of biology is to they rely initially on identifications made by paratax-
produce a complete inventory of all Earth’s biodiversity, onomists (Basset et al., 2004).
including a list of all of species found on Earth and There are crucial consequences of the taxonomic
a comprehensive Tree of Life (Cardoso et al., 2011; impediment in the study of global diversity patterns.
Hinchliff et al., 2015). Many exciting developments in While macro-ecological and evolutionary studies rely on
the last half century, including molecular phyloge- exhaustive lists of species in different geographic re-
netics, phylogenomics, and large-scale natural history gions and biomes, incorrect identifications abound in
collection digitization efforts, have pushed the bound- large databases (e.g., iDigBio, GBIF). Misidentifications
aries of systematics in exciting new ways (Sauquet & in these datasets can lead to significant errors in large-
Graham, 2016). This has resulted in a much more scale studies, including incorrect richness estimates and
Volume 105, Number 3 Lagomarsino & Frost 407
2020 Taxonomy in the Study of Neotropical
Biodiversity
species identity (Cardoso et al., 2017), overestimation of DNA sequence data (Hart et al., 2016), revolutionizing
species richness in poorly explored areas (Maldonado the field of molecular systematics (Chomicki & Renner,
et al., 2015), and inaccurate species distribution models 2015; Iles et al., 2017; Dodsworth et al., 2019), a
(Oleas et al., 2019). Indeed, Cardoso et al. (2017) traditional realm of museum specimens. Further, the
documented up to 40% error rate in non-taxonomically use of degraded DNA from specimens has contributed
verified checklists aggregated from publicly available to other biology subfields such as population genetics
databases. Inaccurate datasets are a clear threat to the (Martin et al., 2016), local adaptation (Exposito-Alonso
accurate understanding of broad patterns of biodiversity. et al., 2018), and microbiome ecology and evolution
Even though they entail significant investments of time (Daru et al., 2018a).
and personnel, every attempt to use large databases in Because of the increased interest in natural history
biodiversity studies should involve detailed taxonomic collections and their associated data, a more diverse
verification and various data-cleaning procedures. array of scientists has been introduced to the inner
workings of museums than ever before. We hope that
HERBARIA AS A SOURCE OF DIVERSE DATA TYPES TO STUDY this has helped museums move away from a long-
THEPAST, PRESENT, AND FUTURE OF BIODIVERSITY standing stereotype that taxonomists are misanthropes
who prefer to work in isolation. This is especially im-
One of the most exciting changes in the study of portant as it is likely that an even broader community of
biodiversity in recent years is a resurgence in the use of end users of collections data will exist in the future
museums and specimen-derived data in a broad range (Schindel & Cook, 2018; Lendemer et al., 2020). It is
of biological inquiry. This has been bolstered by speci- crucial to remember, though, that these creative, often
fic funding programs by the U.S. National Science broad-scale studies that are being undertaken within
Foundation (NSF), including the Postdoctoral Research collections are only possible thanks to the massive
Fellowships in Biology “Interdisciplinary Research Using collecting efforts of the past. In particular, the resur-
Collections,” “Advancing Digitization of Biodiversity gence in floristic research in the 1970s through the early
Data,” and “Planetary Biodiversity Inventories” pro- 2000s led to major growth in Northern Hemisphere
grams. Outside of the United States, the digitization of herbaria, as discussed below. These specimens, and the
historic herbaria in Europe, including the Natural His- taxonomists whose hard-earned specialist knowledge
tory Museum (BM), Royal Botanic Gardens, Kew (K), aided the application of valid names, power most of
the Muséum national d’Histoire naturelle (P), and the the research conducted on the origin and maintenance
Naturhistorisches Museum Wien (W), is of particular of Neotropical biodiversity today. While it is heartening
importance to Neotropical botany; these herbaria hold to see increased interest in natural history collections,
many type specimens and collections by notable early their future utility hinges on the continued investment in
explorers of the Neotropics. In addition to stimulating taxonomy, which represents the foundation for high-
research, this increased investment in collections-based quality biodiversity research (Wheeler, 2020).
research has spurred simultaneous growth and use of large
databases of collections data and images, including iDig-
CONTRIBUTIONS OF HISTORICAL COLLECTIONS TO OUR
Bio (,https://www.idigbio.org/.) and the Global Biodi-
MODERN UNDERSTANDING OF NEOTROPICAL BIODIVERSITY
versity Information Facility (GBIF; ,https://www.gbif.org/.).
The Global Plants database (,https://plants.jstor.org/.) Understanding the origin and maintenance of Neo-
has made type images from around the globe available tropical biodiversity is difficult not only because of the
online; however, while its original intent was to empower complexity of the ecological and evolutionary processes
researchers around the world (especially the Global South) that generated these patterns, but also because of the
with access to these important specimens, institutional fees enormous challenge of simply documenting and de-
now make this a challenge. scribing diversity. Biodiversity documentation requires
The recent emphasis on collections-based research funding and the long-term dedication of teams of tax-
has resulted in a renaissance in biology (Funk, 2018). onomists, knowledgeable field guides, artists, and pho-
We have gained more in-depth understanding of phe- tographers. These efforts are not frequently undertaken;
nology (Hart et al., 2014; Park et al., 2018), morpho- however, major events in the history of Neotropical
logical evolution (McAllister et al., 2018), the impacts of botanical exploration, including significant expeditions,
climate change on plant-animal interactions (Meineke the development of institutions dedicated to the study
& Davies, 2018), and shifting species ranges (Vellend and preservation of biodiversity, floristic projects, and
et al., 2013). These advances would not have been botanical surveys, have shaped much of what we know
possible without the depth of data through space and about the Neotropical flora today.
time granted by collections. Improved molecular tech- Herbarium specimens are the medium through which
niques have also allowed us to generate genome-scale taxonomic and systematic work is accomplished, and,
408 Annals of the
with increased frequency, often form the basis of eco- et al., 2000; Funk & Richardson, 2002; Meyer et al.,
logical and evolutionary studies. Much of the Neotropics 2016; Troudet et al., 2017; Daru et al., 2018b). Most
is under-collected relative to temperate regions, espe- relevant to the data presented above are temporal and
cially given its high species diversity. We examined the collector bias. For example, the time of year in which
degree to which each Mesoamerican and South Amer- collectors tend to go to the field creates temporal bias in
ican country has been botanically explored and docu- natural history records, which can extend into years
mented using the metric of vascular plant collections when collecting activity peaks or plummets (Funk &
per land area (km2; Fig. 1). For comparison, we also Morin, 2000; Norris et al., 2001). These bumper years, as
included this metric for the United States and Spain. demonstrated by our timelines (Figs. 2, 3), often correlate
Costa Rica, by far, has the best-represented flora in with specific projects or expeditions. This may introduce
digitized herbaria among all Latin American countries. collector bias, and, in fact, the majority of collections in
This is undoubtedly due to a long history of botanical many developing tropical countries result from few prolific
expeditions, institutional support, and flora projects in collectors, resulting in an overrepresentation of their pref-
Costa Rica. erences, including proclivities for specific taxa, habitat
To better understand how major events, including types, or regions (Hijmans et al., 2000; Daru et al., 2018b).
floristic projects initiated by Missouri Botanical Gar- Cultural and logistic bias associated with the collection of
den, correlate with increases in herbarium collections, certain taxa or clades over others leads to taxonomic and
and, thus, our knowledge of the plant diversity in those phylogenetic bias (Hortal et al., 2007). For example,
areas, we assembled timelines of collection for selected arachnids, insects, and other invertebrates are underrep-
countries in Central America (Nicaragua, Costa Rica, resented in collections, while birds and angiosperms are
and Panama; Fig. 2) and South America (Venezuela, overrepresented, a trend that has increased over time
Colombia, and Ecuador; Fig. 3). Estimates of the num- (Troudet et al., 2017). Geographic bias, also known as
ber of collections of vascular plants per year were taken “roadside bias,” refers to the higher density of collections
from the number of preserved specimen occurrences made in areas accessible by transportation, like roadsides
reported for Tracheophytes in GBIF. These timelines and riverbanks, and those surrounding major urban hubs
were compared to major events in the history of botan- and institutions, including herbaria and museums (Hijmans
ical exploration for each country, which were confirmed et al., 2000; Funk & Richardson, 2002; Loiselle et al.,
from the literature (Nicaragua: Stevens et al., 2001; 2007). Additionally, each source of bias is accompa-
Montiel & Stevens, 2019; Costa Rica: Polakowsky, nied by a level of taxonomic, geographic, and temporal
1879; Durand & Pittier, 1891; Durand et al., 1893; uncertainty in the associated digitally accessible infor-
Tonduz, 1895; Pittier, 1908; Dodge, 1933; Standley, mation. Biases and uncertainty limit the utility of broader
1937; Jiménez-Luthmer, 1969; Gómez & Savage, 1983; applications (e.g., range maps and niche modeling) for the
McCook, 1999; León, 2002; Hammel et al., 2004; understanding of current biodiversity patterns, complicat-
Panama: Dwyer, 1964; Woodson & Schery, 1980; Moreno, ing future biodiversity projections and the accurate doc-
2004; Venezuela: Huber & Wurdack, 1984; Berry et al., umentation of species composition and distribution patterns
1995; Colombia: Pinto & Ruiz, 1984; Forero, 1988; over time (Meyer et al., 2016; Troudet et al., 2017).
Callejas & Idaŕ raga, 2013; Villamil-Montero & Ming, Beyond an improved understanding of which and how
2016; Diazgranados et al., 2019; Ecuador: Diels, 1937; many species occur in the Neotropics, collectors have
Acosta-Solis, 1969; Wiggins et al., 1971; Renner, 1993; also generated hypotheses about the processes under-
Jørgensen & Le ón-Y ánez, 1999; and the Missouri lying biodiversity patterns. For example, during his
Botanical Garden website: ,http://www.mobot.org/MOBOT/ Andean expedition, Alexander von Humboldt noticed
Research/.). that temperatures decreased as elevation increased,
In each case, major expeditions, the establishment of and, concomitantly, plant species changed (von Humboldt
institutions (e.g., national herbaria, Instituto Nacional & Bonpland, 1807). From these observations, the hy-
de Biodiversidad [INBio] in Costa Rica, the Smithso- pothesis of altitudinal zonation was developed and re-
nian Tropical Research Institute [STRI] in Panama) and mains a topic of investigation to this day (Snowden,
academic programs (e.g., the Organization of Tropical 1933; Johns, 1985; Ohsawa et al., 1985; Druitt et al.,
Studies in Costa Rica), floristic projects, and ecological 1990; Frahm & Gradstein, 1991; Uhlig & Uhlig, 1991;
surveys all had noticeable impacts on the number of Pendry & Proctor, 1996; Kessler, 2000; Sklenář, 2006).
collections made (Figs. 2, 3). These projects and insti- Similarly, Alwyn Gentry is perhaps best known for his
tutions have bolstered our knowledge and understand- long-standing hypotheses regarding the origin and
ing of species numbers, distribution, composition, and maintenance of Neotropical floristic diversity, especially
community assembly of the Neotropical flora as a whole. how it relates to biogeography and landscape change
This understanding necessarily reflects known cul- through time (Gentry, 1982a, 1982b, 1988, 1992). His
tural and logistic biases in biodiversity data (Hijmans taxonomic background (further discussed below) and
Biodiversity
Figure 1. Number of vascular plant collections per land area (km2) for Mesoamerican and South American countries. Number
of collections for each country is based on the number of preserved specimen occurrences of Tracheophyta reported in GBIF
(,https://www.gbif.org/.).
abundant time spent making observations in the field in- Gentry spent substantial time collecting plant speci-
spired his hypothesis that “Amazonian-centered” clades of mens throughout the Neotropics, becoming acquainted
lowland canopy trees and lianas have evolutionary histories with the taxonomic and morphological diversity of the
that contrast with “Andean-centered” clades of mid- to high- flora. He was a consummate taxonomist, especially of
elevation epiphytes, understory shrubs, or large monocots Bignoniaceae, a group he worked on for his entire career
(Gentry, 1982a). This remains a major biogeographic hy- and for which he contributed treatments for numerous
pothesis tested by systematists (Fleming et al., 1987; Clark, floras (Miller et al., 1996). Gentry’s contributions to the
1990; Taylor, 1991; Cuesta-Camacho et al., 2006; Pirie study of Neotropical botany resulted directly from his
et al., 2006; Quijano-Abril et al., 2006; Pennington & Dick, deep taxonomic understanding of this focal group and its
2010; Pinto et al., 2012; Lagomarsino et al., 2017), and has place within the broader context of Neotropical forests.
become so ingrained in Neotropical botany that researchers Many of his insights came from establishing 226 tran-
often present their study systems as “Amazonian-centered” sects (now known as “Gentry plots”) in geographically
(e.g., Macrolobium Schreb. section Macrolobium [(Murphy distinct regions (Phillips & Miller, 2002), allowing him
et al., 2018)], Swartzia Schreb. [Pinto et al., 2012]), or to consolidate his taxonomic and ecological data into a
“Andean-centered” (e.g., Bambusoideae [Clark, 2001], Cen- unified theory of Neotropical biogeography. Begun ini-
tropogon C. Presl [Lagomarsino et al., 2016], Heliconia L. tially as an avenue to understand the ecology of Bigno-
[Andersson, 1989]). Humboldt’s and Gentry’s contributions niaceae (Miller et al., 1996), these plots transformed
exemplify how the powerful combination of taxonomic ex- into a key resource for the understanding of the taxo-
pertise and extensive field observations can drive fields of nomic composition and overall patterns of plant diver-
study for decades or centuries. sity across tropical forests. Arguably, it is Gentry’s
training and efforts as a taxonomist that allowed him
to become not only one of the best tropical plant iden-
IN THE SPIRIT OF AL GENTRY: EXAMPLES OF INNOVATIVE
tifiers who has ever lived, but also one of the most
NEOTROPICAL BIODIVERSITY RESEARCH POWERED BY
important scientific thinkers of the 20th century.
TAXONOMIC KNOWLEDGE
Many researchers or groups of researchers have
Gentry’s hypotheses have stood the test of time and adopted similar approaches to understanding the
laid the foundation for research into Neotropical floris- ecology and evolution of Neotropical plants. These
tics and biogeography that continues through today. researchers first develop taxonomic knowledge and
410 Annals of the
Figure 2. Number of vascular plant collections per year with timelines of selected events for Nicaragua, Costa Rica, and
Panama. Number of collections per year for each country were gathered from the number of preserved specimen occurrences of
Tracheophyta reported in GBIF (,https://www.gbif.org/.) for each year. Events were confirmed from the literature (cited in main
text).
resources for a particular group and, subsequently, use et al., 2013; Thode et al., 2019), and evolution of traits
that knowledge to test large-scale hypotheses in ecology associated with the climbing habit (e.g., Pace et al.,
and evolution. Below, we highlight a few taxonomic 2011, 2015; Sousa-Baena et al., 2014), insect-plant
groups that complement Gentry’s approach to science, interactions (Nogueira et al., 2012, 2015), and pollina-
though it should be noted that many additional groups tion systems (e.g., Alcantara & Lohmann, 2010, 2011),
would be equally well represented below. The prolifer- among others. Across these diverse works on Bignonia-
ation of model clades (Donoghue & Edwards, 2019) to ceae, an in-depth, organismally focused understanding
study Neotropical biodiversity is likely thanks in large of the ecology and evolution of the largest clade of
part to the increased development of methods that Neotropical lianas has emerged. As a result, the Bigno-
facilitate analyses of biodiversity data (e.g., phyloge- niaceae represent as important a clade for understand-
netic comparative methods and species distribution ing the origin and assembly of Neotropical biodiversity
models). and biogeography today as they did when Gentry was
active.
BIGNONIEAE (BIGNONIACEAE)
SOLANUM L. (SOLANACEAE)
Al Gentry’s legacy of Bignoniaceae has been carried
forward, largely thanks to the contributions of Lúcia Despite being one of the largest genera with ca.1500
Lohmann’s group (Universidade de São Paulo, Brazil) species, Solanum is an excellent example of how tax-
in the tribe Bignonieae. Continued descriptions of new onomic research can inform evolutionary research.
species (e.g., Firetti-Leggieri et al., 2015; Frazão & Largely thanks to the leadership of Sandra Knapp
Lohmann, 2018), range extensions (e.g., Brito et al., (Natural History Museum) and Lynn Bohs (University
2018), checklists (e.g., Lohmann, 2010; Lohmann & of Utah), there is a large and vibrant community working
Ulloa Ulloa, 2006), floristic treatments (e.g., Lohmann on various projects related to Solanum and the broader
et al., 2018; Costa et al., 2019), synopses (e.g., Lohmann Solanaceae. Taxonomic work in Solanum, including
& Taylor, 2014; Fonseca & Lohmann, 2019), and mono- monographs, species descriptions, and floras, is incred-
graphs (e.g., Medeiros & Lohmann, 2015; Francisco ibly active (e.g., Barboza, 2013; Stern et al., 2013;
& Lohmann, 2018) are conducted in parallel with Särkinen et al., 2015b; Knapp & Vorontsova, 2016;
studies on the phylogenetics (e.g., Lohmann, 2006; Särkinen & Knapp, 2016; Knapp et al., 2019; Flora do
Kaehler et al., 2019), biogeography (e.g., Lohmann Brasil, 2020). This is paired to frequent phylogenetic
Biodiversity
Figure 3. Number of vascular plant collections per year with timelines of selected events for Venezuela, Colombia, and
Ecuador. Data collection was the same as in Figure 2.
updates (e.g., Weese & Bohs, 2007; Särkinen et al., studies of habitat preferences coupled with new phylo-
2013a, 2015a; Spooner et al., 2018; Martine et al., 2019), genetic data informed taxonomic revision (Daly & Fine,
including macroevolutionary studies (Echeverrı́a-Londoño 2011, 2018; Damasco et al., 2019; Daly, 2020) and the
et al., 2020). Thanks to this relatively complete (though mechanisms underlying habitat specialization and spe-
continually updated) taxonomic knowledge, Solanum rep- ciation (Fine et al., 2013a, 2013b; Misiewicz & Fine,
resents an ideal clade in which to link genomics with 2014; Misiewicz et al., 2020). Additional research in
various components of biodiversity (Knapp et al., 2004). Protium spans many subdisciplines of ecology and evo-
In fact, Andean tomatoes are becoming a model system to lution (Zapata & Fine, 2013; Fortunel et al., 2016;
understand evolutionary processes at play in rapid radi- Vleminckx et al., 2018), demonstrating the reach of
ations (Baek et al., 2016; Pease et al., 2016; Hamlin & taxonomically centered research across subdisciplines
Moyle, 2019; Nevado et al., 2019). Insights from Solanum of biology.
have also played a major role in understanding species
distributions in the Neotropics (Knapp, 2002; Särkinen CHALLENGES TO INCREASING THE REACH OF FLORISTICS AND
et al., 2013b). TAXONOMY
PROTIUM BURM F. (BURSERACEAE)

A major criticism of taxonomy is the field’s lack of
objectivity (Turrill, 1957), a shortcoming that many
Protium is used as a model to study ecological and systematists acknowledge (Strasser, 2019). Responding
evolutionary dynamics of Amazonian trees (Daly et al., to this criticism, statistical methods have been devel-
2012), with an emphasis on edaphic specialization (Fine oped over the past few decades to make systematics
et al., 2004, 2005, 2013b). The ability to initially pose more data-driven. Molecular systematics is a prime ex-
questions in Protium came from a solid foundation of ample: using variation in DNA sequences across species,
taxonomy, in recent years especially by Douglas Daly phylogeneticists are able to apply biologically informed
(New York Botanical Garden) (e.g., Daly, 1989, 1992, models to understand species relationships (e.g., Xi et al.,
2007), complemented by a robust phylogenetic frame- 2012). Species delimitation methods are also catching up
work established by Paul Fine (University of California, to the statistical rigor of phylogenetics, with model-based
Berkeley) (Fine et al., 2005, 2014). In turn, ecological methods (e.g., Zapata & Jiménez, 2012; Yang, 2015)
412 Annals of the
frequently applied instead of, or in addition to, a tax- practices (Nesom et al., 2019). In sum, systematists should
onomic expert’s gestalt. This has resulted in a blooming be considered just as important to answering the major
subfield known as “integrative taxonomy” (Schlick- questions of evolutionary biology, ecology, and conservation
Steiner et al., 2010; Fujita et al., 2012; Prata et al., as experts from other subfields, and should be more com-
2018), which reduces subjectivity and facilitates sta- monly integrated into efforts to understand global biodiver-
bility in classification schemes. As a result, descriptive sity patterns.
taxonomy is becoming a more rigorous discipline
(Sangster & Luksenberg, 2015). Monography, too, is TOWARD AN INTEGRATED FUTURE WHERE MONOGRAPHY
currently in the midst of a 21st century revolution ANDFLORISTICS ARE AT THE CORE
(Reginato, 2016; Zapata, 2018).
An additional major impediment to extending floris- No matter how complex a model or how large an
tics and taxonomic research in recent decades has been assembled database is, there is no replacement for
the difficulty measuring its impact. While tools have organismal understanding, the realm of taxonomists.
been developed to quantify the reach of specimens, Inclusion of taxonomic experts in large-scale studies
including Bionomia (Shorthouse & Page, 2019; ,https:// of global diversity patterns is a crucial step toward
bionomia.net/.), there is a stigma about the limited integrating monography and floristics and centering
reach of museums and their curators. Furthermore, study of the origin and maintenance of Neotropical
floras, monographs, and alpha taxonomic works are biology in organismal biology and diversity. This is
not commonly cited, especially outside of the field of especially important given the current emphasis on
systematics (Werner, 2006; Wägele et al., 2011), even understanding tropical forest diversity and the subse-
when these works are the primary source of data for quent implications for conservation and the mitigation
particular research projects. This results in a reduced of climate change effects (Baker et al., 2017). As we
academic profile for the researchers who conduct continue to become increasingly interdisciplinary, it is
taxonomic research, impacting their career progres- essential that taxonomists are not only seen as a source
sion. Indeed, hiring and promotion decisions, as well of specimen identification, but, given their specialist’s
as nominations for awards and fellowships, are made perspective on organismal biology, also fully integrated
based on metrics including citations (e.g., h-index, into research projects as key members of the team.
i-index) and other non-quantifiable dimensions Long-term ecological plots that add vouchered spec-
of “impact” that are not typically associated with imen distribution information gained in a systematic
herbarium-based researchers, all of which tend to way provide important insight into how the biodiversity
be lower for taxonomists. By devaluing taxonomy, crisis is unfolding in diverse areas, both temperate and
academic culture can stymie the forward progress tropical. These plots are of huge value as they allow for
of the very basic cataloging and description of bio- foundational research into tropical ecology, while con-
diversity that is so critical for steady scientific progress of tributing to the documentation of biodiversity (Condit,
all biodiversity-related research. Citing primary taxo- 1995). They also present an opportunity to link taxon-
nomic literature whenever relevant is important to em- omy to large-scale ecological studies. Given that a large
phasize fairly the importance of this branch of biology, proportion of tropical plant species diversity is thought
while ensuring that research can be replicated. to be undescribed, continued vouchering of these plots
Finally, taxonomists need to do a better job inte- is likely to result in substantial species discovery. In
grating with ecologists, evolutionary biologists, policy fact, taxonomists have already begun to develop floras
makers, and the general public. For example, conver- (Croat, 1978), describe new species and genera (van der
sation with policy makers, both domestic and interna- Werff & Nishida, 2010; Kawasaki & Pérez, 2012), and
tional, is crucial to correctly and respectfully implement publish identification guides (Muñoz et al., 2017) across
protocols in the current complex ecosystem of regula- the many long-term forest plot sites. In turn, these
tions, including the Nagoya Protocol on Access and taxonomic tools allow researchers to more accurately
Benefit Sharing (Rabeler et al., 2019). Further, com- conduct their research, whether they are ecologists
munication with diverse scientists can begin (or con- documenting local processes governing community com-
tinue) with the development of user-friendly floristic position or climate change scientists understanding
treatments and taxonomic tools, including identification patterns of carbon sequestration.
keys and visual floras. Additionally, stability in taxon- Despite the important contributions of forest plots to
omy should be a priority, to the extent that it is possible biodiversity research, collections from plots present
in light of phylogenetic relationships. Taxonomic name biases. For example, plots intended for long-term study
changes, especially to plants important in research or hor- need to be in areas where researchers can access the plots
ticulture, can cause particular uproar (Lowry et al., 2019), repeatedly, often in national parks and natural reserves.
even when they follow taxonomic and nomenclatural best These protected areas likely provide a different picture of
Biodiversity
species composition than the disturbed areas that rep- NSF Dimensions of Biodiversity grant program “As-
resent the most common locations for general botanical sembly and evolution of the Amazonian biota and its
collection (e.g., roadsides and pasture edges; Hijmans environment: An integrated approach” resulted not only
et al., 2000; Funk & Richardson, 2002; Loiselle et al., in important breakthroughs related to understanding the
2007). This results in a mismatch between the habitats for origin and maintenance of Amazonian biodiversity
which we have the most in-depth ecological knowledge through novel fieldwork and extensive museum-based
(i.e., from established plots in forest interiors) and those research (e.g., Weeks et al., 2016; Nazareno et al.,
from which we understand the most about distribution, 2017; Bemmels et al., 2018; Fine & Lohmann, 2018;
morphological variation, and taxonomy (i.e., roadsides). Cracraft et al., 2020), but also in important contributions
Further, sampling is typically restricted to woody plants to a deeper understanding of the poorly known Ama-
above a certain diameter at breast height (DBH), and zonian geological history (e.g., Cheng et al., 2013; Wang
efforts to document herbaceous, lianescent, and epiphytic et al., 2017; Pupim et al., 2019). Another important
diversity in long-term plots are much less common example of ongoing systematic collections efforts in the
(Nieder et al., 2000; Krömer & Gradstein, 2003; Wolf Neotropics is Kew’s Colombia Bio Program (,http://
& Alejandro, 2003; Flores-Palacios & Garcı́a-Franco, colplanta.org/.), which is actively conducting major
2008; Obermüller et al., 2012; Campos et al., 2015), even expeditions to document plant and fungal flora of this
though these plants make up a large portion of species biodiverse country, pairing these with original research
diversity, especially in Andean floras (Gentry, 1982a). and product development, and working directly with
Additionally, many specimens are sterile and thus, in Colombian researchers to engender cultural change
addition to being time-consuming to identify, are of limited toward greater awareness and appreciation of biodiver-
utility to taxonomists (Mori, 1992). We argue that, while sity by the general public and to provide actional rec-
maintaining long-term plots is essential to the study of ommendations that will help Colombia become more
forest dynamics through time and to the basic documen- competitive and sustainable in its use of biodiversity
tation of biodiversity, broader collection outside of the (Diazgranados et al., 2019). Importantly, these efforts
limited number of plots is also essential. explicitly include Colombian researchers and partner-
The continued collection of specimens in a system- ships, including support from regional Colombian gov-
atic and replicable fashion is especially important as ernments, as well as Kew and U.K. government bodies
species distributions shift and species extinction risk (see Acknowledging taxonomy’s colonial history below).
increases. An increased collection of vouchered plant Continued investment in interdisciplinary work that
data requires the input and collaboration of taxonomic is centered around taxonomy, including emphasis on
efforts, particularly if the resulting data are going to be of under-studied taxa or regions, will result in a better
maximal utility to a broad user base (Baker et al., 2017). description of biodiversity and a more in-depth under-
For example, large numbers of accurately identified standing of ecological and evolutionary processes. Ul-
specimens are key to estimating accurate species dis- timately, this support is key to mitigating the effects of
tributions (Feeley & Silman, 2011). In addition to climate change and developing conservation plans that
continued collection, it is also important that taxono- can effectively reduce extinction risks of key species.
mists continue to identify specimens in natural history Here, it is crucial that support be given to taxonomists so
collections. Museum-based research is an important they are able to summarize biodiversity data in com-
source for species discovery: ca. 50% of all species prehensive monographs, develop well-researched floras,
of plants that remain to be described are thought to have and infer the phylogenetic relationships that are so
already been collected and to be sitting in herbaria critical for stable classifications and a deeper under-
waiting to be discovered (Bebber et al., 2010). Unfor- standing of the evolutionary and biogeographical history
tunately, given high levels of ecosystem destruction and of biotas. Only by supporting curatorial efforts will we
biodiversity loss, floras are increasingly becoming a improve our understanding of Neotropical plant diver-
historical record of what once existed, not what currently sity as a whole.
exists (Heywood, 2001). With this in mind, there is no
more important time to invest actively in the curation
ACKNOWLEDGING TAXONOMY’S COLONIAL HISTORY
and growth of herbaria than the present. As May (1992)
noted, there is a time limit to our discipline, and this Finally, any call to revitalize taxonomy in the 21st
time may be approaching faster than we realize. century would be incomplete without mentioning the
Toward this end, it is crucial that governments and importance of decolonizing the field. The history of
institutions continue to support taxonomic research. taxonomy, like allied fields including biogeography
This should not be hard to justify, given that funding (Eichhorn et al., 2020) and field ecology (Baker et al.,
of taxonomically informed biodiversity studies in recent 2019), is rooted in colonial history. Harkening to the
decades has been very productive. For example, the days of Linnaeus, early history of modern taxonomy
414 Annals of the
involved European explorers sponsored by imperialist citations (Fig. 4B, C) using the primary institution that
governments bringing species native to colonial terri- an author is affiliated with as a proxy for their country.
tories back to Europe, where they received a Latin name We subsequently visualized the total number of authors
(Heywood, 1983). Even today, though no longer explic- based in each country in the combined citations across
itly colonialist, European and North American taxono- all eight journals, scaled by each country’s estimated
mists still “discover” and name new tropical species population, using rworldmap (South, 2011). Our results
that have had traditional indigenous names for gener- suggest that Latin American researchers are very active
ations (e.g., Whaanga et al., 2013). Further, taxonomic participants in Neotropical plant taxonomy today (Fig.
infrastructure, including the number of registered taxon- 4) and that they are often part of international collab-
omists and density of biodiversity collections, is under- orations, especially between researchers in the United
represented in megadiverse countries of the Global States and western Europe (Fig. 4B, C). Some Latin
South, including many in the Neotropics, even though American countries (e.g., Brazil, Colombia, and Costa
there are still disproportionate levels of biodiversity left Rica) have proportionally more active researchers pub-
to describe in this region (Paknia et al., 2015; Barlow lishing on Neotropical taxonomy than the United States,
et al., 2018). To increase inclusivity and equity in tax- while others do not have any representation in our
onomy, we must acknowledge this unequal access, con- dataset (e.g., Paraguay, Nicaragua, and Surinam). These
front our painful history, and identify mechanisms in differences could be explained by lack of established
which to center, amplify, and support local perspectives international collaborative collection efforts (as noted
and integrate them into international efforts. A relatively above), differences in national funding of scientific
easy first step (though we admit we do not take it here) is infrastructure in the last decade (Ciocca & Delgado,
to identify and apply alternative terms to refer to the 2017), or differing academic publishing preferences
tropical region of the Western Hemisphere; the “New across countries (Estrada-Mejı́a & Forero-Pineda, 2010).
World tropics,” “Neotropics,” and “American tropics” We also observed differences in the structure of global
all reflect a colonizer perspective. Beyond changing networks that reflect the scope and targeted audience
colonizer-centered terminology, researchers in the of different journals. For example, journals with an
Global North should aim to build capacity in the Latin explicit global focus (e.g., Phytotaxa) commonly have
American countries where they collect specimens and collaboration networks that span multiple global re-
describe new taxa, include authors from those countries gions, including both North America and western Europe
in their research and publications, cite research prod- (Fig. 4B), while regional journals (e.g., Caldasia) have
ucts produced exclusively by Latin American and in- networks centered in the country in which they are
digenous scholars, and explicitly include support for based and tend to not extend to more than one region
Latin American and indigenous researchers in funding of the Global North (Fig. 4C). Overall, these analyses
applications where possible (Eichhorn et al., 2020). demonstrate that researchers based in Latin America
While taxonomy has historically been performed by actively publish on Neotropical plant taxonomy and
white researchers based in Northern Hemisphere insti- form key components of international collaborative net-
tutions, today’s ecosystem of Neotropical taxonomy is works. As decolonization efforts should be collaborative,
notably international. This is likely partially due to
community-accepted undertakings, any future progress
national and international regulation of biological ma-
toward this end will benefit from the fact that Latin
terial in which explicit collaboration with in-country
American voices are already central to Neotropical plant
researchers is a condition of approved research plans.
taxonomy, as well as these existing international collab-
However, we also observe many productive, connection-
orative networks.
based collaborative relationships between researchers
based in Latin America and the Global North (including
POSITIONALITY STATEMENT
ones to which we belong). In order to explore the extent
to which modern Neotropical taxonomy is a global As white citizens of the United States who are trained
enterprise, we explored patterns of authorship in eight as scientists and employed by a major U.S. university,
journals with a focus on botanical taxonomy (i.e., Anales we recognize that we have a platform that is not available
del Real Jardı́n Botánico de Madrid, Brittonia, Calda- to all taxonomists. In both of our careers, we have
sia, Novon, Phytokeys, Phytotaxa, Systematic Botany, worked throughout Latin America and in collaboration
and Taxon). We first downloaded the full citation history with a variety of Latin American botanists, and have
for all papers including the Neotropics as a topic from immensely benefitted from the diverse perspectives that
these journals over the past decade (i.e., 2010–2020) we have encountered in the pursuit of scholarship in
from Web of Science (,http://webofscience.com/.). Neotropical taxonomy. So while we call for the field to
We then used the R package refsplitR (Fournier reflect on the colonial history of the field, we also
et al., 2020) to visualize collaborative networks of these recognize that the present manuscript is an insignificant
Biodiversity
Figure 4. Distribution and networks of authors publishing on Neotropical taxonomy. —A. Global distribution of authors’
institutions on Neotropical botany taxonomic publications from eight targeted journals from a Web of Science search, scaled by
estimated population of each country. Colors represent number of authors per million on a sliding scale from light gray to black;
there were no authors in our dataset from countries in white. —B. Author networks for one journal with an explicitly global reach
(Phytotaxa). —C. Author networks for one journal with an explicitly local reach (Caldasia, a Colombian journal).
step toward realizing decolonization. Considerable American countries and indigenous cultures. It is also
scholarship, including by social scientists and historians, critical that entire research teams acknowledge the past
and input from a diversity of perspectives—especially work of botanists who built the knowledge base from
Latin American and indigenous botanists—are essential which they are able to generate and test broad hypoth-
to effectively develop and communicate best practices eses, as well as the broader historical context in which
in the decolonialization of Neotropical plant taxonomy. those taxonomists operated.
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2020 - Lagomarsino & Frost - The Central Role of Taxonomy in The Study of Neotropical Biodeiversity

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THE CENTRAL ROLE OF Laura P. Lagomarsino2* and Laura A.

* Author for correspondence: [email protected]

PROTIUM BURM F. (BURSERACEAE)

CONCLUSION Literature Cited

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