Mycology
An International Journal on Fungal Biology
ISSN: 2150-1203 (Print) 2150-1211 (Online) Journal homepage: http://www.tandfonline.com/loi/tmyc20
Diversity patterns, ecological associations and
future of research on Costa Rican myxomycetes
Carlos Lado & Carlos Rojas
To cite this article: Carlos Lado & Carlos Rojas (2018): Diversity patterns, ecological
associations and future of research on Costa Rican myxomycetes, Mycology, DOI:
10.1080/21501203.2018.1481153
To link to this article:  https://doi.org/10.1080/21501203.2018.1481153
© 2018 The Author(s). Published by Informa
UK Limited, trading as Taylor & Francis
Group.
Published online: 05 Jun 2018.
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MYCOLOGY
https://doi.org/10.1080/21501203.2018.1481153
Diversity patterns, ecological associations and future of research on Costa Rican
myxomycetes
Carlos Lado a and Carlos Rojas b,c
aDepartment of Mycology, Real Jardín Botánico (RJB, CSIC), Madrid, Spain; bForest Resources Unit, Engineering Research Institute, University
of Costa Rica, San Pedro de Montes de Oca, Costa Rica; cExperimental Interdisciplinary Station of Agroecological Models (FEIMA), University
of Costa Rica, Turrialba, Costa Rica
ABSTRACT ARTICLE HISTORY
The most active research period on myxomycetes in Costa Rica has taken place in the last three Received 5 March 2018
decades. During this time, most of the collections have been carried out and most of the scientific Accepted 23 May 2018
articles have been produced. However, the lack of standard protocols and systematic planning KEYWORDS
across the country generated a need to conduct an analysis of myxomycete records to define Amoebozoa; biodiversity;
future lines of work. A compilation, cleaning, standardisation and analysis of information asso- Central America;
ciated with a database of more than 7800 records that comprised 242 species of myxomycetes conservation; database;
reported in Costa Rica during the last 110 years, was carried out. An interpretation of data with a management; Mesoamerica;
conservation approach that integrated elements of data-mining and geographical information microorganisms;
systems was conducted. Results showed that myxomycetes has been comparatively well studied Myxogastria; slime molds
in Costa Rica in relation to other regional or tropical countries. However, survey effort has been
unequal within the territory, leaving some interesting areas or substrates understudied. The
absence of long-term goals to study this country and Mesoamerica has limited the potential
that the analysed data can have within the context of conservation. This could be the next logical
step in the study of this group of microorganisms in that country.
Introduction comparisons of tropical biodiversity (see Janzen 1988).
However, such artefact of research, product of the avail-
Large-scale biodiversity studies with emphasis on bio-
ability of high-quality biological datasets, may simply
geographical elements are required for several groups
reflect the early establishment and continuous operation
of microorganisms (see Fontaneto and Brodie 2011).
of world-class biological stations in the forests of Costa
However, robust datasets accumulated over time are
Rica.
not available for most of these groups in most parts of
As a logical consequence of the latter, some regions
the world. In the Mesoamerican context, Costa Rica is
of the country have been over studied in comparison
a unique study case for myxomycete analysis given its
with others, thus affecting the generation of objective
research history and development of investigations
comparative systems of biodiversity assessment for
(Rojas and Doss 2013). These efforts may have wider
administrative or ecological units, which rely on more
geographical implications since the regional baseline
standard efforts in each of these individual elements.
knowledge (see Cotterill et al. 2013) has been accu-
This is not only a problem in Costa Rica, and Gotelli and
mulated in that territory.
Coldwell (2001) mentioned that most of the relative
Costa Rica is a country within the Mesoamerican
comparisons of biodiversity among countries, regions,
Biodiversity Hotspot (Brummitt and Lughadha 2003)
2 ecosystems or biomes are constrained by methodolo-with a land surface of 51,100 km and an elevation
gical issues that limit the actual application of such
range between sea level and 3820 m. Its biodiversity
evaluations. In the case of myxomycetes, for instance,
has been comparatively more studied than other regio-
comparisons of diversity across Central American coun-
nal countries due to a combination of political and his-
tries do not reflect natural patterns and are simply the
torical elements as well as infrastructural and academic
product of sampling schemes. For instance, the study
characteristics (see Evans 1999). This country has been
of myxomycetes in Nicaragua, Costa Rica and Panama
used historically as a benchmark to establish
started in the early part of the 1900s, contrasting
CONTACT Carlos Rojas carlos.rojasalvarado@ucr.ac.cr
© 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided the original work is properly cited.
Published online 05 Jun 2018
2 C. LADO AND C. ROJAS
dramatically with incipient myxomycete research in El components, which aid to close the bioliteracy gap
Salvador or Belize, which started in the last 20 years on microscopical organisms.
(see Lado and Wrigley de Basanta 2008; Rojas et al.
2013).
Materials and methods
Interestingly, even within a country like Costa Rica,
well studied in terms of vertebrate and plant biodi- This project was carried out during 2016 and 2017
versity, the effort placed to study groups like the both in the Royal Botanical Gardens of Madrid, Spain
myxomycetes has been far from being evenly distrib- and the Engineering Research Institute of the
uted across the territory. For instance, Schnittler and University of Costa Rica, in the framework of a coop-
Stephenson (2000) carried out a reference study for eration research grant (COOPB20155) funded by the
ecological purposes but mainly focused on tropical Spanish Research Council.
dry areas of the northwestern section of the country, A consolidated database of myxomycete records
thus leaving the rest of the territory understudied. for Costa Rica was compiled from several sources.
This uneven distribution of work is not surprising, These included the herbarium of the National
and it demonstrates that for some microscopic groups Museum of Costa Rica (acronym CR), the herbarium
it is difficult to establish organised systems of study of the University of Costa Rica (USJ) and the Farlow
due to the comparatively low numbers of researchers Herbarium in Harvard University (FH). Additionally,
than for macroscopic organisms. This constraint has data from the personal collection of Martin
obvious effects on conservation efforts, which rarely Schnittler (deposited at Botanische Staatssammlung
include microorganisms in the agenda. München, Germany, acronym M), the myxomycete
Despite the latter, for myxomycetes, Costa Rica collection at the University of Arkansas (abbreviated
does not represent a weak model of integrated as UARK) and the Myxogastrid Biorepository of the
study either. Work has been carried out since the Engineering Research Institute at the University of
1970s, when Alexopoulos and Sáenz (1975) and Farr Costa Rica (abbreviated as INII) were used. These
(1976) started systematising research in this territory. are the collections in the world with most of the
Consequently, the compilation of information and myxomycete records from Costa Rica.
integrated analysis of historical research as well as All actual vouchers deposited at CR, USJ and INII
the determination of future lines of study for Costa were checked individually in the respective herbar-
Rica has lagged the strategies determined for other ium. Information of collections from UARK and M
groups of organisms, but it is ahead of other tropical were checked online and cross-validated with perso-
countries. nal databases from the collectors (Steven L
The present study aimed at the construction of a Stephenson at UARK, Martin Schnittler at M). Data
nomenclatural and ecological database with informa- from FH were checked online in the database of the
tion on myxomycetes from Costa Rica as a strategy herbarium. All collections of myxomycetes were cross-
to promote the concept of standardisation within a checked with a previous database constructed by
conservation framework with a focus on this group Rojas et al. (2010) and the final database was com-
of microorganisms. This is strategic due to the impor- pared, looking for inconsistencies, with a database of
tance of biodiversity research within a context of bibliographic records from the Neotropics constructed
achievable taxonomic goals using standard protocols by the Myxotropic project (www.myxotropic.org).
for prioritising conservation units (see Margules et al. The final database contained information such as
2002). However, such task is only possible through herbarium and collector number, species name, date
deep analysis of information, which is performed of collection, province, county and locality information,
using data-mining and pattern visualisation techni- georeference, elevation, forest type, climate zone infor-
ques. For countries with a recent history of myxomy- mation, substrate, collector and identifier. After the
cete study like Costa Rica, this is very important to consolidation of this unique database, all collecting
provide an answer to logical questions of applied dates were revised and corrected to a standard format
biological research based on previous research pat- to eliminate inconsistencies. For the geographical
terns. Such consolidation of a standardised database work, the independent administrative units known as
also promotes educational and informational “cantones” in Costa Rica have been referred to as
MYCOLOGY 3
counties in this study. Criteria for georeferencing Chiu et al. (2014). Rarefaction curves and diversity
included the use of decimal coordinates and the profiles were created with iNEXT for R (Hsieh et al.
WGS84 datum. Georeferences were assigned to all col- 2016) based on Chao et al. (2014) for both the con-
lections either using the direct information from collec- solidated database constructed herein and a pre-
tors, obtained with a personal GPS unit, or by vious one based on Rojas et al. (2010). For table
establishing centroids associated with localities where creation, species selection was performed consider-
collections were made. In the second case, to minimise ing only those species with dissimilar diversity pro-
possible errors, areas with average elevation within files. Statistical differences observed in contingency
county of collection were used to select centroids and analyses using an alpha of 0.05 were shown in the
additional information in the Herbarium USJ was tables as bolded values.
retrieved from original collecting logbooks. All other
missing elevations were assigned to records in a similar
manner (using geographical centroids for the most Results
accurate location assigned). For substrates, a series of
categories such as bark and wood, ground litter, aerial A database with more than 7800 records of myxomy-
litter, flowers and inflorescences, fruits, lianas, living cetes in Costa Rica was compiled. This dataset con-
cryptogams, living plants, twigs and dungwere created tained 242 species in 40 genera, providing further
and used to standardise the database. These categories evidence of the richness in the Mesoamerican biodi-
are based on the microhabitat separation defined by versity hotspot (see Figure 1). These values represent
Rojas et al. (2014). Bark and wood is the equivalent of around 25% of the myxomycete species known in the
coarse woody debris and living cryptogams is the sub- world, more than double the known species in Cuba,
strate associated with epiphyll myxomycetes. Records the best-known country in the Caribbean biodiversity
associated with living plants were separated from the hotspot, and more than 50% of the species recorded
latter. In the case of all variables standardised in the by Lado and Wrigley de Basanta (2008) for the
database, original information either from the physical Neotropics. The ACE and iChao 1-estimator values
voucher labels or from databases was maintained for for the maximum number of species based on the
reference purposes. Similarly, all collecting numbers current dataset were 274 and 295 species, respec-
assigned by collectors and herbarium numbers tively. The range of possible number of species to be
assigned when vouchers were deposited were main- expected in the country based on the 95% confidence
tained and cross-checked among partial databases. intervals for the iChao 1 estimator was calculated
Nomenclature for myxomycetes was based on Lado between 274 and 325 species. The taxonomic diver-
(2005-2017), forest types were named according to sity index (TDI) was calculated as 5.95 and the overall
Holdridge (1967) with modifications by Ortiz- Shannon’s and 1-D Simpson’s diversity indices were
Malavassi (2014) and conservation areas are named in 4.05 and 0.96, respectively. When compared with a
accordance with local legislation. previous record dataset from 2010 (Rojas et al. 2010)
After that process, a series of analyses were carried when the TDI value was 5.77, results showed rarefac-
out on the database with the objective to summarise tion curves to be similar (Figure 2). This demonstrates
the information and examine patterns. For this part that the previous effort of 4990 records had already
of the study, data-mining techniques were carried explained in detail the pattern of increasing number
out by creating data flow analysis and visualisation of species to be expected (extrapolation on Set_2010).
nodes on KNIME v.3.4 (Berthold et al. 2008). In fact, with a 50% increment in sampling effort (up to
Summarised data from the previous step were either 7500 records), the current dataset (Set_2017) gener-
used to create maps on QGIS v.2.18 (QGIS ated a very similar curve within the boundaries pro-
Development Team 2004-2014) or analysed statisti- vided by the 95% confidence intervals of the first one.
cally on JMP v.10 (SAS Institute 1989-2007). Diversity In an analogous manner, the diversity profiles of both
indices and calculation of ACE and iChao 1 sets (Figure 3) were very similar and showed the
(improved Chao 1) values for the maximum number current dataset to be associated with higher species
of species were performed using Spade in R (Chao richness (associated with q = 0) but lower diversity
et al. 2015). The second one was selected based on index values (q > 1).
4 C. LADO AND C. ROJAS
Figure 1. Map of the central section of the Americas showing the relative location of Costa Rica along with the Caribbean and
Mesoamerican biodiversity hotspots.
Figure 2. Rarefaction curves for the complete dataset considered herein (Set_2017) and a partial dataset considering records made
until 2010 (Set_2010), showing the confidence intervals as shaded areas along the main line and both the inter- and extrapolation
sections with an estimation of 10,000 records.
Records were found in all seven provinces of Costa Nandayure, Naranjo, Orotina, Palmares, Río Cuarto,
Rica but only in 64 of the counties, which represented San Pablo, Tilarán, Valverde Vega and Zarcero.
78% of the 82 administrative units in the country (see Interestingly, some of these are among the counties
Figure 4). The most studied counties were Sarapiquí, with the lowest forest cover in Costa Rica. Table 1
Bagaces, Paraíso and Talamanca, coinciding with shows a summary of counties with numbers of
strong research carried out by Steven Stephenson, records and species associated with them according
Martin Schnittler and the second author of this study to the database built; and the Pearson’s correlation
in the localities of La Selva Biological Station, Palo value between county area size and number of
Verde National Park, Cerro de la Muerte and Cahuita. records was 0.46 whereas with number of species it
The only counties with no records formally assigned was 0.47, showing moderate to weak relationships.
to them were: Abangares, Alajuelita, Cañas, Esparza, Cartago was the only province that showed myx-
Flores, Guácimo, Guatuso, Matina, Moravia, omycete records associated with all its counties.
MYCOLOGY 5
Figure 3. Hill number-based diversity profiles for both the complete dataset considered herein (Set_2017) and a partial dataset
considering records made until 2010 (Set_2010).
Figure 4. Map of Costa Rica showing the location of myxomycete records within the boundaries of administrative counties coloured
according to record frequency. The eight counties with most records are shown at the bottom of the map.
Puntarenas and San José had over 90% of their coun- The distribution of records by geographical location
ties studied, Heredia about 80%, Limón and and historical period within the last 106 years is shown
Guanacaste over 64% and the least studied province in Figure 5. It was clear that most of collections and the
was Alajuela with only 53% of its counties showing broader distribution of collecting locations are asso-
records of myxomycetes. Interestingly, the correlation ciated with the last three decades. Also, the central
between the county-based completeness and the part of Costa Rica seems still to be an important region
relative frequency of records per province was 0.69, for myxomycete research. It is interesting to note that
showing that within provinces some counties were the period with myxomycete research backed up by
partially over studied in comparison with others. deposited collections started in the 1960s, when the
6 C. LADO AND C. ROJAS
Table 1. Summary of county size information and recorded myxomycetes according to the dataset compiled in the present
investigation.
County Area (km2) Total area (% total) Estimated forest cover (%) Myxomycete records Myxomycete species
Alajuela 388.4 0.76 30 4 4
San Mateo 125.9 0.25 30 5 5
San Carlos 3347.9 6.55 25 11 7
San Ramón 1018.6 1.99 45 13 8
Los Chiles 1358.8 2.66 10 11 9
Atenas 127.1 0.25 30 28 11
Poás 73.8 0.14 20 30 11
Upala 1580.6 3.09 30 55 19
Grecia 395.7 0.77 30 227 19
El Guarco 167.6 0.33 45 2 2
La Unión 44.8 0.09 30 2 2
Alvarado 81.0 0.16 30 5 3
Cartago 287.7 0.56 45 34 16
Oreamuno 202.3 0.40 15 33 16
Jiménez 286.4 0.56 60 108 22
Turrialba 1642.6 3.21 70 462 47
Paraíso 411.9 0.81 65 532 63
Hojancha 261.4 0.51 45 1 1
Carrillo 577.5 1.13 45 3 2
Santa Cruz 1312.2 2.57 65 7 6
Liberia 1436.4 2.81 45 91 14
Nicoya 1333.6 2.61 45 119 17
Bagaces 1273.4 2.49 45 634 78
La Cruz 1383.9 2.71 65 414 89
Belén 12.1 0.02 15 2 2
Santa Bárbara 53.2 0.10 15 3 3
San Isidro 26.9 0.05 25 5 4
Heredia 282.6 0.55 45 22 9
Barva 53.8 0.11 25 35 12
Santo Domingo 24.8 0.05 15 57 15
San Rafael 48.3 0.09 25 28 17
Sarapiquí 2140.5 4.19 50 1071 97
Limón 1765.7 3.46 70 5 4
Siquirres 860.1 1.68 70 34 15
Pococí 2403.4 4.70 30 91 22
Talamanca 2809.9 5.50 80 729 66
Garabito 316.3 0.62 70 1 1
Montes de Oro 244.7 0.48 50 1 1
Golfito 1753.9 3.43 50 5 4
Aguirre 543.7 1.06 50 5 4
Buenos Aires 2384.2 4.67 50 123 22
Osa 1930.2 3.78 50 95 23
Parrita 478.7 0.94 30 278 32
Coto Brus 933.9 1.83 50 155 51
Corredores 620.6 1.21 30 533 52
Puntarenas 1842.3 3.61 45 566 89
Coronado 222.2 0.43 50 1 1
Escazú 34.4 0.07 30 1 1
Curridabat 15.9 0.03 15 1 1
Goicoechea 31.5 0.06 30 2 2
Tibás 8.1 0.02 15 2 2
Aserrí 167.1 0.33 50 4 3
Tarrazú 297.5 0.58 40 4 4
Desamparados 118.2 0.23 30 4 4
León Cortés 120.8 0.24 30 7 6
Turrubares 415.2 0.81 70 17 7
Mora 162.0 0.32 50 13 10
San José 44.6 0.09 15 37 12
Santa Ana 61.4 0.12 50 53 17
Puriscal 553.6 1.08 50 119 20
Acosta 342.2 0.67 50 179 26
Dota 400.2 0.78 40 108 40
Montes de Oca 15.1 0.03 30 132 47
Pérez Zeledón 1905.5 3.73 50 497 84
MYCOLOGY 7
Figure 5. Map of Costa Rica showing the location of myxomycete records according to period when collections were made depicted
as coloured categories. The relative frequency of records over time is shown at the bottom of the map.
North American researcher Constantine J. Alexopoulos Most collections have been made in areas with an
teamed up with local professor José Alberto Sáenz. average precipitation between 2000 and 4000 L/m2
Both researchers collected in several locations and pro- (Figure 6) corresponding with the Evergreen Tropical
duced the first consolidated list of Costa Rican myxo- Wet forest type (Figure 7). Few collections (relatively
mycetes (Alexopoulos and Sáenz 1975). speaking) have been made in areas with precipitation
Figure 6. Map of Costa Rica showing the location of myxomycete records within the precipitation zones. The distribution of records
associated with precipitation categories is shown at the bottom of the map.
8 C. LADO AND C. ROJAS
Figure 7. Map of Costa Rica showing the location of myxomycete records within climate regions. The distribution of records
associated with these regions is shown at the bottom of the map.
higher than 6000, lower than 1500 L/m2 (equivalent to Table 2. Numbers of records for selected species of myxomy-
mm) or within the evergreen subtropical humid forest cetes showing associations (in bold) with precipitation cate-
gories according to the database constructed herein.
type. A series of Pearson’s correlations calculated
Annual average Precipitation (L/m2)
between the number of collections from each category 1500– 2000– 3000– 4000–
of precipitation or forest climate region and the relative Myxomycete species 2000 3000 4000 5000
area of the country represented in each category Arcyria incarnata 16 2 7
Arcyria insignis 8 35 7
resulted in a high r value of 0.91 and 0.85 for precipita- Ceratiomyxa morchella 6 1 1
tion and forest climate regions, respectively. The latter Ceratiomyxa 3 3
sphaerosperma
suggested that relative frequency of myxomycete Craterium concinnum 2 14
records was dependent on the area size associated Cribraria costata 7
with both precipitation categories and forest climate Cribraria mirabilis 18Cribraria purpurea 1 19
regions, showing that all categories have been surveyed Diachea bulbillosa 9 1
adequately. Interestingly, the intuitive Simpson’s index Diachea leucopodia 3 3 27 11
Diderma chondrioderma 5
of diversity (1-D) did not follow the same pattern for Lamproderma 12
precipitation (r = 0.52), suggesting that both variables columbinum
Lamproderma muscorum 7
are independent of each other and that some species Leocarpus fragilis 15
may be associated with dryer or wetter regions. Lycogala exiguum 14 1
Macbrideola scintillans 11 1
Table 2 summarises the number of records for some Physarum javanicum 6 1 1 1
species of myxomycetes found to be associated with Physarum serpula 2 30 2
precipitation categories and demonstrates that Arcyria Physarum superbum 5 26 4 3Stemonaria gracilis 13
incarnata, Diachea bulbillosa, Lycogala exiguum and Trichia botrytis 2 11
Tubifera microsperma have primarily been recorded in Trichia decipiens 1 5 11
Trichia favoginea 9 24
dryer areas. Similarly, other species such as Craterium Trichia persimilis 12 1
concinnum, Cribraria mirabilis, Diachea leucopodia, Trichia verrucosa 4 10
Tubifera microsperma 26 1 3
Leocarpus fragilis and Willkommlangea reticulata were Willkommlangea 9
found to be associated with wetter regions. Table 3 reticulata
MYCOLOGY 9
Table 3. Numbers of records for selected species of myxomy- Most of the records were found in old growth forests
cetes showing associations (in bold) with geographical climate
a across the country (Figure 8). Non-forested areas, suc-regions according to the database constructed herein.
cessional forests and open areas accounted all together
Geographical climate region
Myxomycete species NC SC CI CP NP SP CV HN for about 50% of the records. Pearson’s correlations
Arcyria magna 3 calculated between the number of collections from
Cribraria costata 7 each category of forest type and the relative area of
Cribraria mirabilis 18
Cribraria piriformis 3 the country represented in each category resulted in an
Cribraria purpurea 1 19 r value of 0.91. In a similar manner to previous cases,
Diachea bulbillosa 9 1 such a high value suggests that record frequency is
Diderma chondrioderma 5
Didymium listeri 7 associated with the area size of forest type categories.
Lamproderma columbinum 12 When the conservation areas of Costa Rica were
Lamproderma echinulatum 4
Lamproderma magniretisporum 3 used to analyse data, results showed that all conserva-
Lamproderma muscorum 7 tion areas have been surveyed and that the Central
Lamproderma sauteri 2
Lycogala exiguum 14 1 Volcanic Range is where over a third of the records
Macbrideola martinii 17 have been collected (Figure 9). Following the latter, La
Stemonaria gracilis 13
Stemonitopsis aequalis 12 3 Amistad-Pacific, Arenal-Tempisque and La Amistad-
Trichia persimilis 1 12 Caribbean accounted for 40% of all records. The
Trichia verrucosa 10 4 least studied conservation areas were Arenal-Huetar
a Abbreviations: NC: North Caribbean; SC: South Caribbean; CI: Cocos Island;
CP: Central Pacific; NP: North Pacific; SP: South Pacific; CV: Central Valley; North and Tortuguero. In this case, Pearson’s correla-
HN: Huetar North tion between the number of records and the area
encompassed by each conservation area gave an r
shows that most record associations with a geographi- value of 0.43 but did not result in significant differ-
cal climate region were observed for the pacific coast, ences indicating independence between variables
particularly the South Pacific. Interestingly, Stemonaria (P = .20). This result suggests that sampling intensity
gracilis has only been observed in the south Caribbean has been unequal across conservation areas as can be
and Cribraria costata as well as Trichia persimilis showed inferred from the fact that the Arenal-Huertar North
a strong association with the central valley. Conservation Area has the largest percentage of
Figure 8. Map of Costa Rica showing the location of myxomycete records within a simplified scheme of forest type categories. The
distribution of records associated with these categories is shown at the bottom of the map.
10 C. LADO AND C. ROJAS
Figure 9. Map of Costa Rica showing the location of myxomycete records within the boundaries of conservation areas coloured
according to record frequency. The distribution of records associated with these areas is shown at the bottom of the map.
country area with 13% but was only associated with Table 4. Numbers of records for selected species of myxomy-
0.5% of the myxomycete records. cetes showing associations (in bold) with conservation areas
a
The intuitive Simpson’s index of diversity (1-D) according to the database constructed herein.
Conservation area
showed a weak correlation with conservation area
Myxomycete species A B C D E F G H I J K
size (r = 0.31), suggesting independence of variables Alwisia morula 3
and indicating that some species could have regional Ceratiomyxa sphaerosperma 1 5
specificity. Table 4 shows that the two conservation Craterium concinnum 14 2Craterium paraguayense 3
areas with most species unique to a specific region Cribraria mirabilis 18
were Amistad Pacific and Central Volcanic Range. It is Cribraria piriformis 3
Cribraria purpurea 19 1
interesting that a series of species of Cribraria and Dictydiaethalium plumbeum 3
Lamproderma have only been recorded from the first Diderma spumarioides 3
Didymium listeri 7
one, whereas the second area showed unique species Lamproderma columbinum 12
such as Dictydiaethalium plumbeum, Physarum pezizoi- Lamproderma echinulatum 4
Lamproderma magniretisporum 3
deum and Trichia persimilis. The Central Pacific Lamproderma muscorum 7
Conservation Area also showed some unique species Leocarpus fragilis 13 2
such as Didymium listeri and Lamproderma muscorum. Licea castanea 4
Lycogala conicum 2 1
Finally, the distribution of records by substrates Physarum leucophaeum 2 5
demonstrated that most myxomycetes in Costa Rica Physarum pezizoideum 3
Stemonaria gracilis 13
have been recorded in ground litter, bark and wood, Trichia persimilis 12 1
flowers and inflorescences and aerial litter. These sub- Trichia verrucosa 1 4
a
strates accounted for 58%, 24%, 9% and 5% of all Abbreviations: A: Amistad Caribbean; B: Amistad Pacific; C: Arenal
Tempisque; D: Central Volcanic Range; E: Guanacaste; F: Huetar North;
records with substrate information (about 96% of G: Cocos; H: Osa; I: Central Pacific; J: Tempisque; K: Tortuguero
database). Lianas, fruits and dung were the least com-
mon substrates with less than 0.2% of records in all
cases. With these results, most myxomycetes were Physarum didermoides, Didymium bahiense, Physarum
associated with ground litter, bark and wood. compressum and Perichaena dictyonema, which were
However, particularly interesting was the case of recorded on flowers and inflorescences 70%, 58%,
MYCOLOGY 11
42% and 40% of the time, respectively. Arcyria insignis datasets, such as those generated by Schnittler and
was recorded on living plants in a relative frequency Stephenson (2000) for Guanacaste, Monteverde and
of 40% and Perichaena vermicularis on aerial litter, Cahuita or by Walker et al. (2015b) for La Selva
about 30% of occasions. Biological Station, are essential to determine diversity
patterns over time. These areas are good candidates
for future similar studies trying to determine changes
Discussion
in temporal arrangements. However, the execution of
The present study represents an update to the Costa the present analyses also showed that some areas
Rican myxomycete review carried out by Rojas et al. (see below) and forest types (i.e. mangroves, coastal
(2010). All basic calculations associated with biodiver- forests) are undersampled. The latter is not only a
sity increased in the present study in relation to the problem in Costa Rica and may be a general issue in
previous one. Even though such result is not surpris- the northern section of the Neotropics. For this type
ing from an effort-based perspective, since about of analyses, the use diversity profiles could be inter-
2500 new records have been included in the general esting to determine changes in different ecological
database during the last 7 years, it represents an estimators of diversity at different times. This type of
interesting parameter to understand the effect of a figure has the potential to characterise the taxonomic,
sustained effort on general diversity patterns. For phylogenetic or functional diversity of an assemblage
example, the calculated range for the maximum num- (see Chao et al. 2014).
ber of species increased in a logical manner due to an When the record distribution is analysed in terms of
increased number of singletons in the database, counties, it is interesting to observe two patterns. First,
represented by species recorded in the last years most of the poorly studied or overseen counties have
(e.g. Rojas et al. 2015). This result likely affected the low percentages of forest cover in them (see Table 1).
calculation of diversity indices decreasing their value Second, as a consequence of the latter, the number of
in relation to the reference dataset from 2010. myxomycete records and species are independent of
However, as observed in Figures 2 and 3, the general county size and province (also observed in Figure 4).
diversity patterns between such reference and the These results show that most myxomycete research in
present study did not differ dramatically, suggesting Costa Rica has taken place in forested locations and has
that most of the commonly observed morphological not been systematically arranged over spatial or tem-
taxa had previously been recorded. In the context of poral scales (also observed in Figures 5 and 8). Because
Neotropical myxomycete research, these results repre- of the latter, the distribution of substrates observed in
sent a unique opportunity to understand the effect of the database may have also been skewed by limited
sustained studies on biodiversity data. A further eva- sampling schemes. This is a logical result in the first
luation using molecular techniques would be extre- phase of biological research, primarily dedicated to the
mely valuable to assess strengths and weaknesses of documentation of species incidence and distribution.
different techniques for different contexts, but the However, considering that most commonly recorded
value of the data presented herein is the summarisa- myxomycete morphospecies have been likely docu-
tion and standardisation of traditional myxomycete mented in this country, some additional efforts could
work for an entire country. simply focus research in a handful of locations, sub-
In general, the current dataset had an effect strates and forest types, with a systematic approach,
increasing all diversity-based calculations about 8% over moderately longer periods of time. This second
(from 3% for TDI to 12% for species richness) with step of biological research is also important from a
an extra effort that represented 50% of the initial perspective of natural resources management and
effort in 2010. This is important to mention since the environmental policy development (Bergstrom and
current portrayal of myxomycete study in Costa Rica Randall 2016). Independent of the latter, it is remark-
during the last years may represent an interesting able to observe that most myxomycete research has
study case under the scope of global ecological per- taken place in few counties (Figure 4) and only during
spectives such as climate change, habitat disturbance the last decades (Figure 5).
and microbial distribution (e.g. Viscarra Rossel et al. When the analyses of records by precipitation
2014). In this context, for instance, previous regional zones and forest types were carried out, it was
12 C. LADO AND C. ROJAS
interesting but not surprising to observe that most land use over time, it is likely that the actual areas
collections have been made in areas with intermedi- where myxomycetes were collected actually corre-
ate rainfall (Figure 6) in a common forest type such sponded with similar disturbed areas. This is due
as the evergreen tropical wet forest in the country the fact that Costa Rica peaked in deforestation in
(Figure 7). This result can also be observed in Table 2. the middle part of the 1980s (Sánchez-Azofeifa et al.
Since the study of myxomycetes in Costa Rica has 2001) and most collections considered in the present
been locality based and highly associated with study were made after the middle part of the 1990s
national parks or forested areas, it is noteworthy to when disturbed areas were recovering.
mention that even though most records are asso- The latter makes sense for most conservation areas
ciated with areas sharing similar conditions, all forest but does not apply to Arenal-Huetar North, Tempisque
types have been surveyed with an effort proportional and Tortuguero. Figure 9 shows these three to be the
to their relative area. In this manner, species associa- least studied areas in the country for myxomycetes.
tions with some climatic conditions suggest the pat- The first two have traditionally been agricultural
terns seem not to be an indirect product of unequal regions where myxomycete researchers have done lit-
efforts in different climatic regions. As such, they tle work perhaps as a consequence of the difficulty
seem to be real ecological associations, at least at finding accessible forest patches in a landscape domi-
the fruiting body and morphospecies level. nated by private productive lands. However, the lack of
Another support to this idea comes from the results myxomycete research in Tortuguero is intriguing since
of the substrate analysis, which provided further evi- this is one of themost forested and pristine areas in the
dence to the idea of an ecological guild of floricolous country. It is possible that logistic constraints and safety
myxomycetes for tropical areas, as suggested by issues may account for these differences. At the regio-
Schnittler and Stephenson (2002). One interesting nal level, there are also several locations (i.e. Gracias a
aspect of this ecological association is that it seems Dios Department of Honduras, Amazonas Department
not to be influenced as much by landscape-level fea- in Colombia, Guayana Region in Venezuela), where few
tures than by site-level forest characteristics (Rojas et al. or none myxomycete studies have been carried out
2017). In this sense, even though for the general ana- due to similar difficulties.
lysis, the sampling of this type of substrate was propor- In any way, it seems imperative in this moment of
tionally lower than other ones such as wood and bark, myxomycete research in Costa Rica to equilibrate the
results showed a high potential for hypothesis testing effort by establishing surveys in the least studied
studies and conservation approaches. The latter is of regions in a similar manner to what has been done
course magnified within the context of the plant-rich recently. In the partial dataset analysed in 2010 (Rojas
Mesoamerican biodiversity hotspot. et al. 2010), the Arenal Tempisque conservation area
In any way, according to Tables 3 and 4, an interest- was understudied. This result triggered a moderately
ing region for further ecological analyses of potentially sustained effort in the last years, which equilibrated
different assemblages of myxomycetes is the southern research in this area andmade it the third most studied
pacific, which has not received much attention in the in the present study (Figure 9). A similar effort in the
past. The higher elevations in this part of the country Tortuguero conservation area has already been
(between 2000 and 3800 m) seem to host interesting initiated and it is expected to show similar results in
myxomycetes with potential for biogeographical stu- the near future. Also, as mentioned before, research
dies. At the regional level, some integrated studies in effort dedicated to understanding myxomycete inci-
mangroves and costal ecosystems may provide inter- dence on poorly studied substrates (i.e. dung and lia-
esting results for management purposes. nas) or interesting ones (i.e. flowers and inflorescences)
Independent of the fact that most collections have in Costa Rica is necessary, especially after evidence has
been made in forested areas, it is interesting to note shown the distinctive assemblages associated with
that about 50% of all records were associated with some of them (i.e. Wrigley de Basanta et al. 2008).
non-forested areas, successional forests and open In summary, the results from the present study
areas (Figure 8), supporting the idea of richness in show that myxomycetes in Costa Rica have been
non-forested conditions. Even though it is risky to comparatively well studied in the last decades. At
establish such association due to normal changes in the regional and Neotropical level, these studies
MYCOLOGY 13
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