Conserving the Genetic Diversity of Plants

in Austral and Neotropical America

(ANA): A Metanalysis of Published Studies
Using Samples of the Region

M. A. Oliveira-Miranda, A. M. Martino,
R. M. De Oliveira-Miranda, K. Balboa &
M. Aguilera

The Botanical Review

ISSN 0006-8101

Bot. Rev.
DOI 10.1007/s12229-013-9128-5

1 23
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 Author's personal copy
Bot. Rev.
DOI 10.1007/s12229-013-9128-5

Conserving the Genetic Diversity of Plants in Austral

and Neotropical America (ANA): A Metanalysis
of Published Studies Using Samples of the Region

M. A. Oliveira-Miranda1,4 & A. M. Martino2 &

R. M. De Oliveira-Miranda1 & K. Balboa3 &
M. Aguilera1
1
Biodiversidad y Biología Evolutiva, Departamento de Estudios Ambientales, Universidad Simón Bolívar,
Caracas 1081A, Venezuela
2
Centro de Investigaciones en Ecología y Zonas Áridas, Universidad Nacional Experimental Francisco de
Miranda, Coro 4101, Venezuela
3
Instituto de Biología Vegetal y Biotecnología, Universidad de Talca, Talca 3465548, Chile
4
Author for Correspondence; e-mail: oliveira.maria@gmail.com

# The New York Botanical Garden 2002

Abstract Current scientific capacities in Austral and Neotropical America (ANA) for
plant conservation genetics (PGC) were assessed. Publications (1980–2010) were
analyzed, considering the taxa and geographical origin of samples, geographical
origin of the institutional affiliation of the authors (first, corresponding and co-
authors), the threat category of the taxa studied, focus of the genetic analysis
(phylogeny, phylogeography, populations and/or individuals), and focus of the con-
servation actions. Of the 656 publications in conservation genetics, 46 % were about
plants, of which 83 % studied Magnoliophyta. Fourty two percent of publications
concerned five plant families. Twenty seven percent of taxa are threatened and 15 %
are included in the CITES Appendices. Sixty three percent of the publications were
focused on population genetics and 32.6 % on diagnosing threats to the gene pool.
The samples analyzed mainly originated from Brazil and Mexico. Publications are
primarily led by researchers from institutions based in ANA. Over time, PGC
scientific production and proportion of authors from ANA increased.

Keywords Conservation genetics . Austral and Neotropical America (ANA) .

Phytodiversity . Conservation scientific capacity . Scientific production . Plant
conservation genetics

Introduction

The reduction of biological diversity on the planet, as a direct or indirect consequence of

human action, is currently accepted worldwide, not only within the scientific community
but also by the public (Frankham, 1995; Hammer et al., 2003; McFarlane, 2005;
Hoffmann et al., 2010), even more after the Convention on Biological Diversity in
1992. Due to increasing concern, Conservation Biology has emerged as a crisis
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M.A. Oliveira-Miranda et al.

discipline that allows us to understand the driving processes responsible for changes in
the abundance and/or distribution patterns of biodiversity mainly due to anthropogenic
factors, and develop strategies to minimize their consequences (Soulé, 1985).
Conservation biology is by nature a multi-disciplinary field, and amongst the different
disciplines that this science needs to include in order to achieve its goals, population
genetics is becoming more important. The need to incorporate new techniques to assess
the status of a population genetic pool is increasingly agreed upon among conservation
biologists. These tools are included in the area that Soulé and Wilcox (1980) named
“Conservation Genetics.” The main goal of conservation genetics is the study of the
molecular biodiversity in natural populations stressed by human impact (Solé-Cava,
2004). Determining the level of genetic diversity in endangered populations is the first
step towards assessing the risk of genetic variation loss, as a consequence of reductions
in population size or increased inbreeding; both demographic conditions which could
potentially lead endangered populations to extinction (Frankham, 1995; Lehman, 1998;
Loew, 2002; DeSalle & Amato, 2004; Godoy, 2009).
One of the main goals of the genetic conservation approach is to provide essential
information in order to manage populations, maintaining an “acceptable” level of
genetic diversity, whose loss could have a severe impact on their fitness (see O’Brien,
1994; Lehman, 1998; Laikre, 1999). Taking into account the lessons learned from
domestic breeding, together with observations of the loss of genetic variability in
natural populations stressed by over-exploitation, suitable management strategies can
be developed. In order to achieve this goal, it is important to acknowledge that
conservation genetics should develop, or incorporate from other fields, techniques
that take into account patterns and processes and provide a cohesive approach that
must feed decision-making protocols (DeSalle & Amato, 2004). One of the tech-
niques that conservation genetics would benefit from is genomics (DeSalle & Amato,
2004; Allendorf et al., 2010). The advantages that genomics offer for investigating
the genetic basis of adaptation and speciation have become very clear (Bonin, 2008)
and some authors are promoting the transition from conservation genetics to conser-
vation genomics (Allendorf et al., 2010; Frankham, 2010; Ouborg et al., 2010a, b).
The knowledge of genetic diversity is substantially improved by the development
of more and better molecular techniques (Amos & Balmford, 2001; Loew, 2002).
Nevertheless, some works have cast doubts upon its real contribution towards
developing strategies in biodiversity conservation (Vernesi et al., 2008; Kramer &
Havens, 2009).
The ANA region (ANA; Austral and Neotropical America, from Mexico to
Argentina, including Caribbean countries) (Rodriguez et al., 2006; Ceballos et al.,
2009) has a heterogeneous natural and cultural landscape, with an outstanding
biodiversity, taking into account that at least six of countries are considered as
megadiverse (Mittermeier et al., 1997; Aguilera et al., 2003), and seven biodiversity
hotspots are located in ANA (Ceballos & Brown, 1995; Myers et al., 2000). After the
declaration of the Convention on Biological Diversity (CBD), it became the obliga-
tion of each country, especially those considered megadiverse, to increase knowledge
of their biological diversity. The problem is that 70 % of megadiverse countries are
neither included in the group of the most industrialized countries, nor have large
Gross National Product incomes to invest in the basic research needed in this area
(Ceballos et al., 2009). This constraint forces conservation biology researchers in
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Plant Conservation Genetics in Austral and Neotropical America

ANA to make a huge effort to obtain economic resources for infrastructure, devel-
opment and training to improve the knowledge of their biodiversity (Michelangeli
et al., 2004; Rodriguez et al., 2005, 2006; Ceballos et al., 2009), thereby affecting the
development of research in genetic conservation. Molecular genetic techniques are
more accessible and affordable every day (DeSalle & Amato, 2004) and it should be
expected that, despite these difficulties, ANA countries could take advantage of this
knowledge and fulfill their responsibilities in their biodiversity research programs
over time, reinforced by the terms of the CBD through the accession of genetic
resources in each country.
In order to identify the size of the gap between investment and knowledge in the
ANA countries, it is of interest to follow the evolution and emphasis in the develop-
ment of knowledge in conservation genetics in the region. It is of the utmost
importance to identify what, where and who is working on topics related with
genetics applied to conservation in the ANA countries (Rodriguez et al., 2006).
This assessment will hopefully provide the necessary information to determine
how large the gap is between the conservation work that needs to be done, and the
availability of professionals and resources for conservation genetics in this region,
given the socioeconomic limits that many of the ANA countries face, as highlighted
in other studies related with conservation biology (Rodriguez et al., 2006), tropical
ecology (Stocks et al., 2008) or systematic biology (Michelangeli et al., 2004).
Under this scenario, the main aim of this paper is to analyze the actual capabilities
of ANA countries to develop research on their genetic diversity, with emphasis on
their regional phytodiversity, in order to improve their conservation capacity.

Methods

To assess current scientific capacity in conservation genetics in Austral and

Neotropical America (ANA), a search was performed using Web of Science
(apps.webofknowledge.com), including studies published since 1980 until
December 15th 2010. The total number of articles published in 2010 is not complete
due to a delay in their detection in the databases, sometimes even until March of the
next year. The search was performed by looking simultaneously for keywords that
included the names of ANA countries in English and Spanish and the terms “con-
servation genetics” or “genetic diversity and conservation.” Austral and Neotropical
America is often perceived as being united by the Spanish language (Gordon, 2005),
and somtimes called Latin America. In fact, it consists of countries where Portuguese,
English, French, and hundreds of indigenous languages are spoken (Gordon, 2005).
The criteria to select a publication for analysis were: a) at least one author works in
ANA institutions, or b) the source of biological material is located in ANA. We also
included studies with authors located in ANA although the species under study was
not distributed in ANA, in order to know the level of expertise acquired in the area of
conservation genetics, which could potentially be returned to ANA countries.
For each publication the following was recorded: i) country or geographical region
of collected or analyzed samples, ii) the name of the first author; iii) the country of the
institutional affiliation of the first author; iv) the name of the corresponding author; v)
the country of the institutional affiliation of the corresponding author; vi) the
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institutional affiliation of first and corresponding authors; vii) presence of other

authors and their countries of institution affiliation; viii) the year of publication; ix)
journal name; x) main taxonomic group and plant family that belongs the sample
under study; xi) type of analysis, which was divided in: phylogeny, phylogeography,
populations and/or individuals; xii) identification of the research according to the
Conservation Framework Action (Salafsky et al., 2002); xiii) the level of threat or
endangerment following IUCN nomenclature (IUCN, 2010) and category on CITES
(CITES, 2011) of the species under study; xiv) type of organism according to its
exploitation condition (wild or genetic resource), and its geographic origin when the
species is under exploitation: native genetic resource (NGR) or introduced genetic
resource (IGR). For IGR only studies about populations which have been naturalized
were taken into account (Benton, 2004; Earle, 2011; Guiry, 2011; Hechenleitner
et al., 2005; Jenner, 2006; Koenemann & Jenner, 2005; Mapula-Larreta et al.,
2008; Martin & Davis, 2001; Nelson, 2006; Putnam et al., 2008; Shultz, 2007;
Stevens, 2001; Tree of Life Web Project, 1995; Tropicos.org, 2011).
The publications that were suitable were organized using six wide geograph-
ical regions as a reference, following the convention proposed by the Society of
Conservation Biology (SCB) and adopted by several authors (Rodriguez et al.,
2005, 2006): Africa (AF), Austral and Neotropical America (ANA), Asia (AS),
Europe (EU), North America (NA) and Oceania (OC). ANA includes all
countries from Mexico to Argentina and the Caribbean. For the purposes of
this publication NA was considered to be Canada and the USA only. We further
subdivided ANA into three non-overlapping sub-regions: i) NeoA (Neotropical
America), comprising all continental countries from Mexico to Brazil and
Bolivia; ii) AusA (Austral America), comprising Chile, Argentina, Paraguay
and Uruguay; and iii) Caribbean, comprising Cuba, Jamaica, Hispaniola,
Puerto Rico, Lesser Antilles, and Trinidad &Tobago. Furthermore, Neotropical
America was internally divided in two blocks: North (from Mexico to Panama)
and South (from Colombia to Brazil and Bolivia).
In order to assess the effort and amount of work performed in ANA by ANA
researchers the three main aspects considered in the analysis were: i) the geographic
region where the samples were collected; ii) the geographic region of the institutional
affiliation of the first, corresponding, and co-authors of the studies; and iii) the level
of genetic analysis, joined with the approach in a Conservation Framework Action for
plant conservation genetics.
Statistical associations were assessed with contingency tables to compare the
regional patterns and trends that could obtained at different time periods. All the
contingency tables were tested with a chi-square test following Preacher (2001).

Results

Taxa Studied

The initial search produced 1,211 entries. After an exhaustive review, only 656
publications met the defined criteria. These were focused on species from 3 king-
doms: Plantae (46 %), Fungi (0.6 %) and Animalia (53.4 %). Only 1.2 % of the
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Plant Conservation Genetics in Austral and Neotropical America

publications simultaneously evaluated more than one taxonomic group above family
level. Table 1 shows the number of studies on conservation genetics performed on the
three biological kingdoms mentioned before. It is notable that flowering plants
comprise more than 80 % of the plant studies. Because publications on plant
conservation genetics in ANA formally start in 1991, all data was analyzed after that
time.
Among the main Families identified, only five of them, representing 8 % of the
total number of families detected in this study, cover 42 % of publications (see
Fig. 1). Three families belong to the Division Magnoliophyta: Fabaceae, Poaceae
and Solanaceae, and two to the Division Pinophyta: Pinaceae and Araucariacae. It is
noteworthy that almost all studies are limited to few species within a family (Fig. 1).
The Family Araucariaceae is an extreme case, where 16 studies were restricted to two
species. Furthermore, only 29 % of the plants studied can be considered as wild, with
no recognized human use, while 68 % were classified as NGR, having uses ranging
from ethnobotany to commercial and 7 % were introduced plants (IGR), mainly of
commercial interest, that have gone through a process of adaptation to the region
(ANA). Studies of commercial cultivars were excluded. Fifteen percent of all species
considered in the publications that were suitable are included in the CITES appendi-
ces (3.7 % in Appendix Table 4, 9.4 % in II, and 2 % in III) (CITES, 2011). From the
point of view of threat status, 27 % of the studies concerned species at risk of
extinction, while 73 % do not appear on the IUCN Red List (IUCN, 2010).

Geographical Distribution of Research Effort

The samples used in the publications were grouped as following, taking into account
its geographic origin as described before: 83 % coming from Neotropical America,
9 % coming from Austral America, 2 % coming from Caribbean, and 6 % from
different countries throughout ANA (Fig. 2). Figure 3 shows the distribution of
publications done with ANA samples sorted by ANA countries. Samples from
Brazil and Mexico comprised more than 50 % of all studies developed in ANA,

Table 1 Publications in
Taxonomic groups Publications (N) Proportion in
conservation genetics (1980–2010)
Kingdom Plantae (%)
performed on Austral and
Neotropical America (ANA)
Kingdom Plantae 303
Division
Chlorophyta (algae) 1 <1
Rhodophyta (algae) 2 <1
Cycadophyta 7 2.3
(cycads)
Pinophyta (conifers) 42 13.9
Magnoliophyta 251 83.0
(flowering plants)
Kingdom Fungi 4
Kingdom Animalia 349
Total 656
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M.A. Oliveira-Miranda et al.

Fig. 1 Distribution of publications using ANA samples in plant conservation genetics. Families are
ordered (from top to bottom) in Divisions Cycadophyta (first), Pinophyta (2nd–4th) and Magnoliophyta
(5th–19th). Inside each Division, the families are arranged alphabetically

followed by Chile (6.3 %), Costa Rica (6 %), Peru (6 %) and Argentina (5.7 %). In
6.9 % of the studies it was not possible to identify the country where the sample came
from. In most of these cases the publications were reviews.
Regarding the geographic origin of the institution where the first author is asso-
ciated (Fig. 4), it is observed that more than 60 % of studies performed with samples
of subregions NeoA, AusA, and Caribbean have first authors associated to ANA’s
institutions. However, when the origin of samples is from countries of two or more
subregions of ANA, this proportion decreases to less than 40 %. The observed profile
of geographical origin of institutional affiliation of first authors on NeoA, AusA and
all ANA, differs significantly (χ2=15.5, p=0.017), the AusA countries having a
higher participation of first authors affiliated to European institutions; this participa-
tion of European authors becomes higher when studies are focused on regional
studies (throughtout all ANA) (right column on Fig. 4).
When the geographical origin of institutional affiliation of the corresponding
authors was examined (Fig. 5), we observed a similar pattern as for first authors
(χ2=26.5, p=0.000), where corresponding authors of ANA institutions represent
more than 60 %, and the European participation is higher in AusA compared with
NeoA. However in this case, for regional studies (right bar on Fig. 5) the proportion
of corresponding authors associated with ANA institutions decreases whereas the
proportion of researchers from Oceania becomes higher (Others in Fig. 5).
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Plant Conservation Genetics in Austral and Neotropical America

Fig. 2 Relative geographic origin (%) of samples used in publications of plant conservation genetics
(1991–2010), discriminated by ANA subregions. NeoA Neotropical America, AusA Austral America,
Caribbean Caribbean countries, ANA Austral and Neotropical America (studies with samples for different
subregions of ANA)

Furthermore, statistically significant differences were found inside of Neotropical

America (χ2=8.75, p=0.013), between northern and southern blocks.
When we evaluated the coauthors in studies of plant conservation genetics from
ANA, the geographical origin of coauthors reveal variations (Fig. 6), but no statisti-
cally significant difference is observed. The portion of studies performed by foreign
authors is higher when samples come from Neotropical America or when studies
considered samples from multiple subregions of ANA (right bar at Fig. 6). Inside
Neotropical America there are differences again between the northern and southern
blocks (χ2=9.08, p=0.011), the proportion of studies limited to foreign co-authors
being higher in the north of NeoA (29 % vs. 14 %), while the opposite tendency is
observed for studies limited to local co-authors, being higher in the Southern block
(64 % vs. 48 %).

Fig. 3 Distribution at national level of studies using ANA samples in plant conservation genetics (1991–
2010). Ar Argentina; Br Brazil; Ch Chile; CR Costa Rica; Mx Mexico; Pe Peru; Bo Bolivia; Co Colombia;
Ec Ecuador; Gu Guatemala; Others countries with less than 3 % of publications
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M.A. Oliveira-Miranda et al.

Fig. 4 Geographic origin of the institutional affiliation of the first author in plant conservation genetics
publications (1991–2010), considering the geographical origin of samples in ANA. NeoA Neotropical
America, AusA Austral America, ANA Austral and Neotropical America. NA North America (USA and
Canada), EU European Union, Others Africa and Oceania. ANA at right bar represents studies done with
samples from more than one subregion of ANA

Scientific Production Over Time

In order to analyze the trends of scientific activity, considering the geographic origin
of first authors, corresponding authors, and co-authors over the total period 1991–

Fig. 5 Geographic origin of the institutional affiliation of the corresponding author in plant conservation
genetics publications (1991–2010), considering the geographical origin of samples in ANA. NeoA Neo-
tropical America, AusA Austral America, ANA Austral and Neotropical America, NA North America (USA
and Canada), EU European Union, Others Africa and Oceania. ANA at right bar represents studies done
with samples from more than one subregion of ANA
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Plant Conservation Genetics in Austral and Neotropical America

2010, we defined three sub-periods: i) 1991–2000, ii) 2001–2005, iii) and 2006–
2010. After 2000, there is a noticeable, almost exponential increase in the number of
publications, reaching 160 publications in the period 2006–2010 (Fig. 7). Table 2
shows the number of first authors, corresponding authors and total group of authors
classified by region for these periods. The analysis allowed identification of signif-
icant differences in the geographical origin of institutional affiliation of the first
author, corresponding author and geographical composition of the co-authors in the
publications for the periods evaluated (1991–2000: χ2=9.518, p=0.049; 2001–2005:
χ2=12.463, p=0.014; 2006–2010: χ2=15.8, 0.003). The proportion of first authors
from ANA increased from 46 % (in the 90’s) to 71 % (2006–2010). Similarly, the
proportion of corresponding authors from ANA increased from 40 % (in the 90’s) to
69 % (2006–2010). The main change in the composition of coworker teams was the
increase of publications with researchers from ANA only, versus a decrease in teams
with only foreign researchers (Table 2).
Brazil, Mexico, Costa Rica, Argentina, Chile and Peru comprised 74 % of studies
on plant conservation genetics for the period 1991–2010. Brazil, Argentina and Chile
follow the trend described above for first author, corresponding authors, and co-
authors, when all data was analyzed (Appendix Table 4); however, this trend does not
hold for Costa Rica and Peru. In the last 5 years, these two countries showed a
reduction in the proportion on first and corresponding authors associated to ANA
regions, despite the fact that these countries showed high proportion of first and
corresponding authors belonging to ANA, for the three periods considered.

Fig. 6 Relative geographical origin of collaborators in plant genetic conservation studies (1991–2010),
considering the geographical origin of samples in ANA. NeoA Neotropical America, AusA Austral
America, ANA Austral and Neotropical America, ANA & Out institutional affiliation of contributors is
both, inside and outside of ANA, Out institutional affiliation of all authors is outside of ANA. ANA at right
bar represents studies done with samples from more than one subregion of ANA
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M.A. Oliveira-Miranda et al.

Fig. 7 Papers published in plant

conservation genetics in Austral
and Neotropical America during
the period 1991–2010

Furthermore, Costa Rica showed an absolute reduction of publications in plant

conservation genetics in the last 5 years. Also, it is remarkable that in publications
developed with samples from Peru, first and corresponding authors were from NA.
The main change over time was in the composition of co-authors; recently 78 % of
publications include scientists from ANA versus the 37.5 % detected in the 1990s.

Institutions Involved in Scientific Productions

Analyzing the affiliations of first and corresponding authors, we find that Brazil,
followed by Mexico, represent the largest number of institutions involved in publi-
cations related with plant conservation genetics (Table 3). In order to understand the
relationship between institutions and productivity in plant conservation genetics, we
calculated the ratio between the number of institutions associated to first and corre-
sponding authors and the number of publications where at least one co-author comes
from ANA. Brazil, Argentina and Chili are countries that show a better relationship
between institutions and productivity (Table 3).
In a qualitative analysis of the type of institutions where these studies were
performed, it was found that Universities contribute the most number of publications
in plant conservation genetics (>60 %), and the research centers associated to
Universities are next in number of contributions.

Table 2 Geographical origin of institutional affiliation of first authors, corresponding authors and coau-
thors composition of studies performed with ANA’s samples over the time

Year Publications First author Correspondence author Co-authors team

(n)
ANA NA EU Others ANA NA EU Others ANA Out ANA &
ANA Out

1991-2000 50 23 13 12 2 20 16 11 3 16 17 17
2001-2005 98 65 13 17 3 62 15 19 2 46 18 34
2006-2010 153 108 21 23 1 105 24 24 0 91 21 41
301 196 47 52 6 187 55 54 5 153 56 92
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Journal Categories in Studies

The papers included were published in 44 journals. Of these, 43 % of the journals

published more than three publications about plant conservation genetics (87 % of
analyzed publications) and 57 % published less than three studies. When we consid-
ered only journals with more than three publications, we found that 36 % of studies
are in journals oriented toward genetics, systematics and evolution, and represent the
highest proportion of journals (n=9). Twenty five percent of studies were found in
conservation journals (n=4), 20 % on taxon oriented journals (n=6), 12 % in
agricultural and forestry journals (n=3), and 7 % in a general journal.
One noticeable point is that in the case of Brazil, scientists are publishing in
national journals (20 % of all periodical publications with articles on conservation
genetics of plants are Brazilian, and 20 % of all publications analyzed in this study
were performed with samples from Brazil). For other countries, like Mexico, the
tendency to publish papers in national journals was not the same. So while Brazilian
scientists publish their results mainly in national journals, other countries, including
Mexico, are using international journals.

Level of Genetic Analysis, and Position in a Conservation Action Framework

In Fig. 8 the percentage of publications classified by type of genetic analysis is

shown. It is noticeable that almost 63 % were focused on population genetics. Of
these, 65 % were related to species considered as NGR. Furthermore, the rise in
number of publications in all types of genetic analysis (Fig. 9) revealed the same
performance observed for all publications analyzed (Fig. 7), especially for those
related to population genetics papers.
Regarding the focus defined in the Conservation Action Framework (according to
Salafsky et al., 2002) that we could identify in the selected papers, we can observe in
Fig. 10, that 32.6 % of the studies tried to identify how threats influence the genetic
pool of a particular species or population; this is followed by 21 % of the publications
concerning target identification. It is noteworthy that other very important conserva-
tion actions, like defining and evaluating strategies, are represented in a very low

Table 3 Conservation capacities (measured as number of institutions participating) at Austral and Neo-
tropical America for performed studies of plant conservation genetics

Countrya Total publications Publications with at ANA’s institutions Proportion

per country (n) least one author from of first & corresponding institutions/ANA’s
ANA (n) authors (n) publications (%)

Argentina 20 17 7 41.2
Brazil 100 96 51 53.1
Chile 22 18 5 27.8
Costa Rica 21 21 3 14.3
Mexico 75 65 13 20.0
Peru 21 15 2 13.3

a
The six countries that comprehend 75 % of scientific production were analyzed
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M.A. Oliveira-Miranda et al.

percentage of the papers, while use of genetic tools to execute strategies is absent in
the selected publications. If we analyze the trend over time (Fig. 11), it is observed
that if there is an overall increase in the numbers of publications for any of the
conservation actions identified, the action “Identifying threats” shows the fastest
increase; while “Defining Strategies” shows the lowest increase. Finally, NGR
species represented 69.8 % of the papers related to “Target identification” and
58.6 % of the papers related to “Identifying threats”.

Discussion

First of all, it is important to mention that although our analyses were performed on
information gathered from one of the most complete databases available, it is likely
that some non-indexed journals on the Web of Science were not considered, implying
that this analysis should be further complemented with similar searches on additional
databases, like EBSCO and Cambridge Scientific Abstracts.
In addition, it is possible that the number of articles analyzed represents an
underestimation of the scientific production in ANA, even in the case of ISIWeb,
because studies in conservation genetics of plants may not include the keywords that
were used. However, the underestimation should be negligible, since very general
words such as genetic diversity and the names of the countries were used. That the
initial number of papers obtained in the search conducted was double the final
number of studies suitable for this analysis provides evidence for this. Likewise,
studies performed with ANA samples were discarded when they were focused only
on development of molecular techniques, and did not include genetic analyses. That
does not mean that these works will not be important to conservation studies a
posteriori.
In relation to the data obtained, the bias towards studies on Magnoliophyta species
is remarkable but not surprising. This is the group with the largest number of

Fig. 8 Level of genetic analysis of publications produced with ANA’ samples in plant conservation
genetics (1991–2010)
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Plant Conservation Genetics in Austral and Neotropical America

Fig. 9 Level of genetic analysis of publications produced with ANA samples, considering three periods of
time

representative species amongst terrestrial plants. However, in this case the difference
in proportion of studies of conservation genetics on both divisions, in relation to the
number of species recognized in each Division is remarkable (7.2 % for Pinophyta
versus 0.2 % for Magnoliophyta). A possible explanation is that this group includes a
large number of species with economic value and 86 % of them are under a category
of threat. Seventy one percent of the studies with Pinophyta fall into both categories,
species with a high economic value and under extinction risk. In the case of Fabaceae,
Poaceae, Bromeliaceae and Solanaceae, the most studied families amongst
Magnoliophyta, 74 % have some human use (NGR), 9 % are threatened and only
7 % are considered useful and threatened.
The difference between richness in species in different families and the number of
studies performed in each family, seem to be determined by two main factors: i) the
degree of interest in the use of a particular species, and ii) the level of threat of the

Fig. 10 Focus of Conservation Actions (according Salafsky et al., 2002) of publications produced with
ANA samples in plant conservation genetics (1991–2010)
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M.A. Oliveira-Miranda et al.

Fig. 11 Focus of Conservation Actions (according Salafsky et al., 2002) of publications produced with
ANA samples considering three periods of time

species studied, as the analysis of the Conservation Action Framework indicates. Other
factors that may contribute to this pattern could be the special taxonomic and/or
evolutionary interest of a species group, the existence of well consolidated research
groups or research lines that show a high rate of publication, interest promoted by large
international agendas that drive conservation priorities (Rodriguez et al., 2007) and also
financial support the of research (Stocks et al., 2008). Finally, it should be noticed that
access to financial resources for research is limited in many ANA countries, adding
some pressure to the choice of study subjects (Michelangeli et al., 2004).
Regarding the origin of the samples used, although in studies of ANA subregions
the affiliation of authors is mainly with ANA institutions (>60 % of the papers
published), the results indicate that the capability of ANA authors to develop studies
at large geographical scales in ANA is limited. This is shown by their reduced
contribution to studies that attempt to perform analyses over a scale greater than a
single sub-region within ANA (Fig. 6). The reasons behind this pattern could be
financial, lack of or weak relationships between research groups from different
biogeographical areas (different subregions) or problems with obtaining genetic
resource access permits (Michelangeli et al., 2004).
Within ANA region, Brazil and Mexico were the countries that had the most
publications in plant conservation genetics. Since both are mega-diverse countries
and have developed capabilities to perform studies with molecular genetics in
conservation, either with internal research groups or collaborations with research
groups outside of ANA, it is not surprising that they have a greater number of
publications. A similar trend was found by Michelangeli et al. (2004) in their study
of use of molecular techniques in plant systematics in Latin America. This study
made in 2002, showed that Mexico led the number of publications in plant molecular
taxonomy, followed by Brazil.
However, in the present study, Brazil, the biggest country of ANA region, leads the
number of publications with ANA samples, most of them obtained into the country.
Likewise, this can bias the interpretation of a possible collaboration between scien-
tists of different countries inside the same subregion, because Brazil covers so big a
surface that include the distributions of a lot of species living in the Neotropics.
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Plant Conservation Genetics in Austral and Neotropical America

On the other hand, the number of studies inside subregions increased in the later
period analyzed (2006–2010), simultaneously with the number of studies with
foreign authors, particularly in Mexico. Maybe this can be understood as the result
of the fact that some researchers have migrated to North America and the European
Union.
Other megadiverse countries such as Peru, Costa Rica, Colombia and Venezuela
have a very low number of publications in plant conservation genetics. These
countries have not been as successful as Brazil or Mexico, either in developing the
capacity to perform the studies internally or to establish the necessary collaborations
with non-ANA countries to perform research in conservation genetics. This is clear
from the number of institutions in these countries that were involved in the studies
evaluated. Additionally, these countries have to cope with very strict regulations on
permits to access genetic resources and/or a very poor implementation of mechanisms
to obtain such authorizations (Grajal, 1999).
Although the key search was performed to identify studies in genetic diversity and
conservation, the proportion of studies published in specialized journals on these
subjects, considering only journals with more than three studies, is 30 %. This may be
due to the existence of a small number of journals related with conservation (21 % of
mentioned selection) and the emergence of new journals focused on theoretical topics
(47 % of this selected group) which analyze the applicability of the results of crisis
disciplines (e.g. conservation biology, genetic conservation, alimentary production)
to solve specific problems. There is also a general tendency to publish in journals
where the taxonomy and systematics are the main objectives regardless whether
studies are focused on phylogeny, phylogeography, molecular demography or other
areas (32 % of selected group) and in many cases these studies aim to resolve genetic
and evolutionary questions. Intriguingly, an important proportion (16 %) of publica-
tions was observed in journals focusing on agricultural production and forestry,
despite the fact that the search criteria did not include forestry as a key factor. This
is indicative of the interest in research on wild species with potential use for some
kind of production; which is supported by the fact that 68 % of the publications
retrieved were focused on species with recognized uses. Again, it is important to
stress that this analysis excluded studies focusing on plants under production; the
selection was centered on populations of species found in the wild or in gene banks
for maintenance of plant diversity.
The results also show that the main type of genetic analysis represented in the
papers of conservation genetics in plants is population genetics, reflecting a growing
concern about the genetic status of many species, both for wild and NGR sources, as a
consequence of fragmentation and overexploitation. But it is worrying that genetic
tools, especially with molecular markers, are still not widely applied to develop
strategies to monitor illegal trade, for example. It is necessary that researchers go
toward research where they can define objectives on conservation genetics and
evaluate their success, in order to achieve the genetic diversity conservation goal.
Examples of these kinds of studies are evaluation of germoplasm banks in order to
assess their representativeness on the genetic diversity of a type of crop. In the
analysis that was performed, it is noteworthy that many studies related with NGR
and IGR species are related with the maintenance and right identification of germ-
plasm banks (Debouck et al., 1993; Krishna et al., 2004; Rao, 2004).
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M.A. Oliveira-Miranda et al.

This study shows that there is an increasing number of researchers with an

institutional affiliation to ANA involved in the study of the local genetic diversity,
its conservation and the potential use of their species as resources, without causing
damage to genetic pool of the species. Notably over the last 10 years, local re-
searchers have run, led and formed working groups to study plant genetic diversity
in their countries. This was displayed by the increasing number of publications
carried out by ANA research groups, decreasing the dependence on research groups
outside ANA and also by the slightly increasing collaboration between ANA and
Non-ANA researchers in studies totally performed by external researchers. However,
this pattern is highly asymmetrical and only very few countries reach it (Brazil, Chile
and Argentina), so there is still much work to do in order to increase the current
capacity for performing research on plant conservation genetics in the region. A
similar pattern was found by Stocks et al. (2008) in relation to tropical ecology
research. Moreover, the observed pattern did not differ from the one outlined by
Michelangeli et al. (2004) for research in plant molecular systematics, who, as in the
present paper, found that Brazil involved more first author affiliated to institutions of
ANA region, while Mexico involved more researchers from outside ANA.
Our results pointed out that Universities contribute with the largest number of
publications in plant conservation genetics followed by research centers associated to
main Universities. This is opposite to the trend that was observed in forest genetic
resources, in which the research is mainly driven by state research centers (Salcedo
et al., 2009).
Strategies to reduce this asymmetry could be: to improve and encourage collabo-
ration between research groups in the different countries of ANA, to encourage the
exchange of researchers and/or students in order to develop research and training
programs including conservation genetics, promote national and international
agendas that allow access to adequate financial resources for the development of
conservation genetics of ANA biodiversity, build and support a network of exchange
of information among ANA countries, like ReGeneC, and/or make the process of
acquiring the permits of genetic resources access within ANA countries less burden-
some, amongst others. Similar considerations were made by Rodriguez et al. (2005,
2007) in relation to conservation biology programs to be developed in ANA countries
in order to promote researcher training programs in this area.

Conclusions

Most of the studies performed on plants within ANA, related to the topics of conserva-
tion genetics and genetic diversity of wild species, are focused on organisms with
identified uses. In particular, in the case of conifers, the studies also are aimed at species
under threat of extinction. Although most of these studies are conducted and organized
by ANA researchers, the proportion of studied taxa and available research institutions is
not enough to address questions to effectively survey and generate the necessary
information on the genetic diversity of plant species in the region. This is the
case of Brazil, which presents the largest number of studies in their flora,
according to the survey performed in this work. It is also necessary not only
to maintain researches related to population genetics, but to also improve
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Plant Conservation Genetics in Austral and Neotropical America

genetic tools and research to develop conservation actions to monitor the plant
genetic diversity in ANA region. Our results indicate that there is a clear trend
to close the gap between local scientific capacity and the study of the
phytodiversity in the ANA region, but there is still a lot of work to be done
considering that more than 60 % of the neotropical mega-diverse countries
present less than 10 taxa as objects of study in plant conservation genetics.

Acknowledgments We are grateful to Omar Cornejo, who provided many suggestions to the article and
was a great help in revising the text. To Ana María Kelly and Dominique Noome for helping us to revise the
English text. To Angelica Cibrian for the invitation to the Symposium on Conservation Genetics held in
Chile and to be part of this initiative. To the friends who helped us get access to the papers we were unable
to obtain either in Venezuela or Chile. This work was done within the framework of the activities of the
Latin American Network for Conservation Genetics (ReGeneC).

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Appendix

Table 4 Number of papers published in plant conservation genetics from six ANA countries, discrimi-
nated by regional origin of the first author, corresponding author, and coauthor teams, through the period
1991–2010

Origin of Periods Publications First author Corresponding author Co-authors team

samples
ANAa NAb EUc Others ANA NA EU Others ANA Other Ana &
Other

Argentina 1991–2000 7 4 2 1 3 2 2 3 2 2
2001–2005 4 2 1 1 2 1 1 2 1 1
2006–2010 9 8 1 8 1 7 2
Brazil 1991–2000 7 5 1 1 5 1 1 2 2 3
2001–2005 31 29 1 1 29 1 1 24 7
2006–2010 62 56 1 5 57 1 4 51 2 9
Chile 1991–2000 2 2 1 1 1 1
2001–2005 9 3 2 4 3 2 4 1 2 6
2006–2010 11 8 1 2 8 1 2 8 1 2
Costa Rica 1991–2000 3 1 2 1 2 1 2
2001–2005 13 8 2 2 1 8 2 3 5 3 5
2006–2010 5 3 2 2 3 5
Mexico 1991–2000 13 6 2 4 1 6 2 4 1 5 5 3
2001–2005 20 16 2 2 15 3 2 14 1 5
2006–2010 42 25 9 7 1 25 9 8 20 10 12
Peru 1991–2000 8 3 3 1 1 2 4 2 2 3 3
2001–2005 4 2 2 3 1 2 2
2006–2010 9 2 4 3 1 5 3 1 1 7

a
Austral and Neotropical America: from Mexico to Argentina, including Caribbean
b
North America: Canada & USA
c
European Union