Towards an Integrated Approach of Conducting Fungal Research in Costa Rica - revistas. una. ac. cr

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Towards an Integrated Approach of Conducting Fungal Research in Costa Rica - revistas. una. ac. cr
ISSN Electrónico: 2215-3470                   UNICIENCIA Vol. 33, N° 1, pp. 101-117. Enero-Junio, 2019
DOI: http://dx.doi.org/10.15359/ru.33-1.8                     URL: www.revistas.una.ac.cr/uniciencia
                                                        Correo electrónico: revistauniciencia@una.cr

                         Towards an Integrated Approach of
                         Conducting Fungal Research in
                         Costa Rica
              Hacia un enfoque integrado de investigación micológica en Costa Rica
           Em direção a um enfoque integrado de pesquisa micológica na Costa Rica

                       Carlos Rojas-Alvarado                                        Randall Valverde-González
                    carlos.rojasalvarado@ucr.ac.cr                                    valverde1589@gmail.com
             Instituto de Investigaciones en Ingeniería y                    Instituto de Investigaciones en Ingeniería
          Finca Experimental Interdisciplinaria de Modelos                           Universidad de Costa Rica
                            Agroecológicos                                               San José, Costa Rica
                      Universidad de Costa Rica                             Orcid: http://orcid.org/0000-0002-4041-5476
                         San José, Costa Rica
            Orcid: http://orcid.org/0000-0002-7968-4833

                                Recibido-Received: 22/feb/2018 • Corregido-Corrected: 4/jun /2018.
                               Aceptado-Accepted: 13/ago/2018 • Publicado-Published: 31/ene /2019.

        Abstract
        Costa Rica is a small country in Central America with a recent history of fungal research. However, comparative
        differences with other territories in the Mesoamerican Biodiversity Hotspot region have promoted the study
        of fungi and the integration of fungal information with natural resource management. Even though there is
        still a large number of multidisciplinary aspects to cover in Costa Rica for robust incorporation of fungal data
        in conservation and political and developmental agendas, regional advantages have allowed this country
        to move towards such goal more rapidly than other countries in this part of the world. Mycoliteracy-centered
        and citizen science initiatives seem to be the next step in order to normalize disparities in fungal perception
        across regions within the country and promote social interaction with fungi. However, in general terms, the
        Costa Rican society seems to be aware of the potential of fungi as a source of food and medicines and their
        remarkable contribution through ecosystem services. In this manner, fungal conservation and management
        seem easier to conduct in this territory than in other regions of the world where less information on fungi
        has reached the general population.
        Keywords: bioliteracy; Central America; fungi; natural resources
        Resumen
        Costa Rica es un país pequeño en la región centroamericana, con una reciente historia de investigación
        micológica. Sin embargo, algunas diferencias comparativas con otros países de la región biológica

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   Uniciencia es una revista de acceso abierto/ Uniciencia is an Open Access Journal.
ISSN Electrónico: 2215-3470
                                                                                DOI: http://dx.doi.org/10.15359/ru.33-1.8

    mesoamericana han promovido el estudio de los hongos y su integración con el manejo de los recursos
    naturales. Aun cuando todavía existe un sinnúmero de elementos por cubrir en Costa Rica, para una
    incorporación robusta de datos micológicos en la conservación y el desarrollo de agendas políticas

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    sobre recursos naturales, algunas ventajas regionales han permitido que este país avance hacia tal
    objetivo más rápidamente que otros. Iniciativas de micoalfabetización y ciencia popular parecen ser los
    siguientes pasos para normalizar desequilibrios en la percepción sobre los hongos, que tienen diferentes
    regiones en Costa Rica, con el propósito de instar interacciones con estos organismos. No obstante, en
    términos generales, la sociedad costarricense parece estar más atenta al potencial de los hongos como
    fuente alimenticia y medicinal, al igual que a reconocer el rol de dichos organismos de facilitar servicios
    ecosistémicos. De esta forma, la conservación de hongos y su manejo parecen ser más fáciles de llevarse
    a cabo en este territorio que en otras áreas del mundo, donde mucho menos información sobre ellos ha
    llegado a la población general.
    Palabras claves: alfabetización biológica; Centroamérica; hongos; recursos naturales.
    Resumo
    A Costa Rica é um país pequeno localizado na região centro-americana, com uma recente história de pesquisa
    micológica. Porém, algumas diferenças comparativas com outros países da região biológica mesoamericana
    têm promovido o estudo dos fungos e sua integração com o manejo dos recursos naturais. Ainda que
    exista inumeráveis elementos a serem cobertos na Costa Rica para uma incorporação robusta de dados
    micológicos na conservação e no desenvolvimento de agendas políticas sobre recursos naturais, algumas
    vantagens regionais têm permitido que este país avance em direção a este objetivo mais rapidamente do
    que outros. Iniciativas de alfabetização micológica e ciência popular parecem ser os seguintes passos para
    normalizar desequilíbrios na percepção sobre os fungos existentes em diferentes regiões da Costa Rica,
    com o propósito de instar interações com estes organismos. Não obstante, em termos gerais, a sociedade
    costarriquenha parece estar mais atenta ao potencial dos fungos como fonte alimentar e medicinal, assim
    como ao reconhecimento do papel de estes organismos facilitarem os serviços ecossistêmicos. Desta forma,
    a conservação de fungos e seu manejo parecem ser mais fáceis de serem levados a cabo neste território do
    que em outras áreas do mundo, onde muito menos informação sobre eles chegaram à população geral.
    Palavras-chaves: alfabetização biológica; América Central; fungos; recursos naturais.

   T
           he study of fungi in Costa Rica is                        the history and potential of this discipline
           very recent in comparison with other                      for integrated future research with applied
           countries in the world. Even for stan-                    benefits for Costa Rica and other countries
    dards within the Neotropical region, myco-                       with similar conditions. This paper also fo-
    logy in Costa Rica became established later                      cuses on the attempts to carry out interdisci-
    than in other territories. However, the cu-                      plinary and multi-institutional mycological
    rrent extent of mycology and the develop-                        work in Costa Rica with support from pu-
    ments of the last three decades have allowed                     blic Costa Rican institutions.
    Costa Rican mycology to be recognized in-
    ternationally. This review briefly examines

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          102
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    The Multidisciplinary Extent of                                  ta Rica´s School of Biology (García, 2009),
    Fungal Research in Costa Rica                                    is remarkable in this sense since he founded
                                                                     the mycology section at that venue during
           Fungi have been said to be more di-                       the 1960s. Some decades later, however,

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    verse in tropical regions (Aime and Brear-                       the local researchers Marissia Nassar, Ana
    ley, 2012), but estimates on the number of                       Victoria Lizano, Luis Diego Gómez-Pigna-
    potential species in these areas of the planet                   taro, and Julieta Carranza were responsible
    have yet to be revised (Hawskworth, 2012).                       for training the current generation of Costa
    Modern techniques of study have created                          Rican mycologists. Currently, Priscila Cha-
    a revolution in both the rate of description                     verri and Melissa Mardones carry out their
    of new species and the use of fungi for                          work as part of highly-qualified internatio-
    bioprospective research. Ironically, most of                     nal teams.
    the tropical regions in the world, particular-                          Even though the history of mycologi-
    ly in Africa, still lack basic elements to cope                  cal study in Costa Rica is very recent, the
    with the increasing demand to study fungi                        development of mycological research in
    (see Gryzenhout et al., 2012). The most                          this territory has been more prominent than
    important of those elements is perhaps the                       in other countries within the Central Ame-
    availability of qualified personnel conduc-                      rican region (see earlier prominent studies
    ting research according to local interests. In                   such as Singer and Gómez-Pignataro 1984;
    Latin America, for example, some countries                       Gómez-Pignataro, 1996). Such a result is a
    such as Costa Rica have had such human                           partial product of a strong research-orien-
    element present during the last 50 years or                      ted academia, better comparative research
    so, and mycological research, albeit limited                     infrastructure than other regional countries,
    in some ways, has rapidly progressed du-                         political stability, and more developed his-
    ring this time.                                                  torical-professional networks. The develop-
           As it was the case in many other terri-                   ment of research on myxogastrids, a group
    tories, earlier studies of fungi in Costa Rica                   of amoebae once considered part of the fun-
    focused on the documentation of terrestrial                      gi, is an example of that type of coordinated
    macroscopic forms (i.e., Rowlee, 1924; Ste-                      effort taking place in Costa Rica during the
    vens, 1927; Gray and Dodge, 1934). More                          last 50 years (Rojas and Doss, 2013).
    complex analyses were carried out later                                 Estimates show that there are about
    (i.e., Farrow, 1954; Denison, 1963; Bazan                        3,800 species of fungi recorded in Costa
    and Segura, 1970), but still within the fra-                     Rican lands (Obando, 2007). This number
    mework of biodiversity studies. Foreign                          accounts for about 6% of what it is expec-
    researchers have conducted most of these                         ted in Costa Rican territory and about 5% of
    studies, but these studies have allowed the                      what it is known in the world today (Obando,
    Costa Rican academy to develop an interest                       2013). As a reference, the Global Transboun-
    in mycology. The latter derived in profes-                       dary Conservation Network (www.tbpa.net)
    sional training that allowed local resear-                       acknowledges that the Mesoamerican Biodi-
    chers to start developing research projects                      versity Hotspot, where Costa Rica is located,
    independently. For instance, the effort of                       may have up to 10% of the global biodiver-
    the local researcher José Alberto Sáenz, a                       sity. Considering that fungi in most of the
    founding member of the University of Cos-                        regional territories have not been studied as

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    much as in Costa Rica (even in some of the                       The effort of the research team at this insti-
    biodiversity-rich southern states of Mexico),                    tution allowed the characterization of about
    the potential biodiversity values for the Me-                    50,000 specimens of fungi during that time
    soamerican region are remarkable.                                (Vargas, 2016). These specimens protect

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
           Of course, the importance of biodi-                       the biochemical and genetic components of
    versity studies relies on the use of data for                    fungal biodiversity according to Costa Rica
    conservation decisions and policy develop-                       legislation and are currently deposited at the
    ment (Margules et al., 2002) in an integrated                    National Herbarium of Costa Rica (CR) as
    manner with socioeconomic development                            natural heritage of the nation. Along with
    and research initiatives. According to Can-                      the collection of about 5,500 fungal spe-
    tú-Salazar and Gastón (2013), a discrepancy                      cimens at the CR Herbarium (Armando
    between biodiversity-rich areas and lands                        Ruiz-Boyer, pers. comm.) and approxima-
    designated for protection does have a strong                     tely 16,000 specimens at the University of
    negative impact promoting truly effective                        Costa Rica Herbarium (Mitzi Campos, pers.
    public conservation efforts. In developing                       comm.), Costa Rica has the largest scientific
    regions like Mesoamerica, such discon-                           collection of fungi in Central America with
    nection may have enormous consequences                           about 1.4 specimens per square kilometer of
    when ecosystem services and bioprospec-                          terrestrial land. As a collateral reference of
    tion studies are considered. In Costa Rica,                      the work carried out on fungi, Costa Rica is
    the Biodiversity Law (Ley 7788, 1998) de-                        also one of the best studied tropical coun-
    fined in article 7 that fungi are part of bio-                   tries in the world in relation to myxogastrids
    diversity, and therefore fungal resources                        (Rojas et al., 2010), with about 25% of the
    are fully regulated by law in Costa Rican                        global diversity of these organisms (Lado et
    territory. The simple addition of the word                       al., in prep).
    “fungi” in such law has promoted both fun-                              Currently, fungal research in Costa
    gal research and fungal conservation efforts                     Rica still covers the basic biodiversity as-
    within the country. Even though there is sti-                    pect (Desai et al., 2016, Coronado-Ruiz et
    ll much work to do, Costa Rica counts on                         al., 2018). However, applied bioprospec-
    an attractive model of integrated biological                     tive studies have gained momentum (Ro-
    conservation when compared with other                            jas-Jiménez et al., 2016; Lee et al., 2016)
    regional countries. As such, the chapter on                      after the work of Giselle Tamayo in the Na-
    biodiversity in Costa Rica´s periodic report                     tional Institute of Biodiversity (see Gámez,
    about the state of the nation includes an es-                    2007). Ecological studies dealing with fun-
    timate of fungal biodiversity and guidelines                     gal dynamics are rare but have also been
    for fungal conservation (see Obando, 2013).                      carried out in the last years (Rojas and
           This connection between fungal re-                        Calvo, 2014; Rojas et al., 2017; Looby and
    sources and government policy in Costa                           Treseder, 2018). Fungal studies for agri-
    Rica was promoted rapidly with the work                          cultural purposes, the focal point of my-
    carried out by the researchers Milagro Mata                      cological research in Costa Rica for many
    and Loengrin Umaña at the National Insti-                        years, are still conducted in this territory
    tute of Biodiversity (INBio, www.inbio.ac.                       (Marín-Chacón et al., 2017; Castro-Chin-
    cr), between 1989 and 2015, when the most                        chilla and Umaña-Rojas, 2017, McGee et
    recent conservation legislation was created.                     al., 2018), and medical mycology has been

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    recently approached for applied purposes                         recognize the existing links between fungal
    (Jaikel-Víquez et al., 2015). Interestingly,                     components of nature and their own per-
    one of the few ethnomycological studies                          sonal life. For instance, unfamiliarity with
    carried out in Costa Rica was also conduc-                       the role of fungi for soil health in terrestrial

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    ted recently (Molina-Murillo et al., 2015).                      ecosystems, a traditional function of fungi
            Mycology has greatly expanded its                        on the planet, carries on importance when
    range of application across multiple disci-                      soil management is not considered in pro-
    plines in Costa Rica during the last decades.                    ductive lands. The deprivation of soil fun-
    It is simply expected for this trend to conti-                   gi by extensive soil compaction or overuse
    nue in the development of future research.                       of external nutrients creates an imbalance
    Mycology in Costa Rica has evolved to be a                       in fungal populations that influences the
    multidisciplinary field, and fungi have been                     rest of the ecosystem (see Garbeva et al.,
    acknowledged to be important for lifestyles                      2011) and increases dependence on external
    and modern integrated approaches to mana-                        inputs. In Costa Rica, significant differen-
    ge natural resources such as forests (Moli-                      ces in the activity of soil microorganisms,
    na-Murillo and Smith, 2016). There are still                     including fungi, have been documented in
    several fields of applied study and multiple                     different productive systems. These records
    opportunities to promote the integration of                      have shown that intensive agricultural prac-
    fungal resources with other aspects of mo-                       tices have a strong negative effect on the ac-
    dern life, such as food security, human heal-                    tivity of microorganisms in the soil (Sibaja
    th promotion, and engineering or industry                        et al., 2018).
    applications. Along with the development                                The simple understanding of natural
    of computer science modeling using fungi,                        processes involving fungi and the provision
    these areas represent, the direction where                       of ecosystem services, mediated by the di-
    most of the mycological efforts would pro-                       fferent species within the group, are still ne-
    bably yield quantifiable results for the Costa                   cessary in most parts of the world, including
    Rican society in this part of the 21st century.                  Costa Rica. Recent multidisciplinary approa-
                                                                     ches involving specialists in education, tou-
    Comparative Fungal Dynamics in                                   rism, biology, public policy, and conserva-
    Costa Rican Forests and Potential                                tion have been set up and will be tested in
                                                                     the upcoming years. From a biological pers-
    for Integrated Management Stra-
                                                                     pective, strong ecological documentation of
    tegies                                                           fungal species and assemblages over time is
                                                                     necessary. However, the design of the latter
          Fungi are essential for ecosystem                          type of studies should also consider national
    functioning (Dighton, 2016), and services                        priorities and regional inequalities to also
    provided by working ecosystems are pivotal                       promote some socioeconomic development
    elements of development and lifestyle for                        during its execution.
    human societies (Newbound et al., 2010).                                Ecological studies on fungi are critical
    However, due to a modern personal dis-                           to reaching tangible conservation guidelines,
    connection from natural elements of their                        since analyses at the ecosystem level, where
    surroundings (Nisbet and Zelenski, 2011;                         fungi are essential, show the importance of
    Rojas et al., 2016), most individuals fail to                    the group more prominently. In Costa Rica,

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    most of this type of studies have been ca-                       der examination. One of the general areas
    rried out in the last three decades. Examples                    was a seasonally dry forest and the other
    of this are the early efforts of Bills and Poli-                 a premontane wet forest with macroclima-
    shook (1994) who studied leaf litter fungal                      tic differences in rainfall, temperature and

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    dynamics, focusing on fungus-epiphyte asso-                      cloud cover. For this reason, all plots were
    ciations, and Lindblad (2000) who examined                       instrumented with temperature, atmosphe-
    the host specificity of wood-inhabiting fungi.                   ric humidity, and luminosity loggers; and
    More recently, Halling and Mueller (2005)                        hemispherical photographs were obtained
    examined macrofungal associations with                           for canopy cover characterization perfor-
    Quercus forests, Puschendorf et al., (2006)                      med every three months. At the same in-
    studied the relationship between chytrids and                    terval, field surveys of macrofungi and a
    amphibian declines, and Del Olmo-Ruiz and                        characterization of carbon stocks were ca-
    Arnold (2013) documented endophytic fungi                        rried out in all plots. A complete soil cha-
    dynamics associated with ferns.                                  racterization was also performed for all fo-
           Interestingly, one of the patterns ob-                    rest types. The most important results were
    served in these studies is that they have fo-                    summarized in Rojas and Calvo (2014) and
    cused on across-kingdom taxonomic rela-                          Rojas et al., (2017).
    tionships rather than ecosystem dynamics.                               Overall, the two forest patches in the
    Even though the former documentation is                          seasonally dry forest showed lower tree
    important for scientific purposes, such re-                      density values, lower canopies, and less vo-
    search does not necessarily generate outco-                      luminous trees than premontane wet forests.
    mes that are translatable into information                       Similarly, average ground biomass and car-
    for human societies to grasp, digest and                         bon dioxide equivalent units per hectare, an
    apply. This phenomenon is a partial con-                         estimate of potential contribution to carbon
    sequence of higher education training in                         neutrality programs, were lower in the sea-
    Biology, in which curricular structures tend                     sonally dry forests. The average temperatu-
    to neglect socioeconomic implications (Ba-                       re value in the dry forest was 26.6±4.1 ver-
    zzul, 2014). In this sense, within biological                    sus 16.6±1.6 in the premontane wet forest;
    or environmental sciences, few studies have                      and average humidity was 73.6±18.1 versus
    been produced in Costa Rica where fungi                          78.5±19.9 for the same comparison. Canopy
    are documented within the framework of                           dynamics, average number of seedlings,
    ecosystem service provision and potential                        and luminosity were more variable in the
    socioeconomic impact on local societies.                         seasonally dry forests than in the premon-
           During the period 2011–2014, resear-                      tane forests. From a forestry perspective,
    chers at the Engineering Research Institu-                       carbon stock-related and microenvironmen-
    te of the University of Costa Rica started                       tal values looked better in the premontane
    a monitoring project intended to evaluate                        wet forests despite significant differences in
    the dynamics of fungal populations in the                        temperature (but not in humidity). Howe-
    context of forest performance. For this pro-                     ver, when the fungal component was inclu-
    ject, two areas in the country were selected,                    ded in the analysis, results showed a more
    where two different 25- to 30-year-old fo-                       complex scenario.
    rest sections of 0.2 ha were studied, for a                             Macrofungal dominant forms in the
    total of four different forest biosystems un-                    seasonally dry forests were classified in the

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    genera Collybia and Marasmius, whereas                           also explained, in detail, the diameter of the
    Laccaria and Lactarius dominated the pre-                        pileus and the hymenial area to biomass ra-
    montane wet forests, and no differences in                       tio for the complete dataset suggesting that
    the number of fruiting bodies or total fun-                      the functional variability of macrofungal

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    gal biomass per hectare were found. In ge-                       populations was associated with forest per-
    neral, soil and wood-associated macrofungi                       formance. In this case, when fungal data was
    had larger reproductive structures but were                      included in the analysis, it was clear that a
    less heavy, in terms of dry weight, in the                       simplistic forestry-based only perspective
    seasonally dry forests than in the premon-                       would only provide a partial perspective of
    tane wet forests. These results were interes-                    the complete story. Interestingly, when all
    ting since dominant forms in seasonally dry                      the variables calculated in the study were
    forests were mostly saprophytic, whereas                         analyzed over time, differences were obser-
    dominant forms in premontane wet forests                         ved in 2012 versus other years, particularly
    were mostly mycorrhizal. Even though my-                         for the macrofungi documented in the pre-
    corrhizal forms were significantly heavier                       montane wet forests. Considering that 2012
    than saprophytic ones, the allocation of bio-                    was a wet La Niña year on the Pacific coast
    mass resources also differed among these                         of Costa Rica, results suggested that macro-
    two. Macrofungi in forest patches with hi-                       fungal assemblages in the premontane wet
    gher carbon-stock values allocated less re-                      forests (mostly mycorrhizal) were less resi-
    sources in the production of hymenial areas                      lient than those in the seasonally dry forest.
    than macrofungi in forests with lower car-                       It is imperative to study these results more
    bon values. The relationship between a hy-                       thoroughly for management of natural re-
    menial area and dry weight was 3.34 mm2/g                        sources (Figure 1) since they suggested that,
    for mycorrhizal versus 8.26 mm2/g for sa-                        despite the lower carbon-stock value, seaso-
    prophytic fungi. Interestingly, the latter                       nally dry forests in Costa Rica also function
    measurement showed strong correlations                           as resilient environments for microorganis-
    with temperature (r=0.99), light intensity                       ms inhabiting them, fungi among them. In
    (r=0.94), and canopy openness (r=0.99).                          addition, these results also showed that the
    Even though most visually appealing for-                         less resilient mycorrhizal assemblages, a
    ms (mycorrhizal) were present in premon-                         potential source of food, require a differen-
    tane wet forests, the ecosystem service,                         tial management approach.
    provided in the form of decomposition by
    the more diverse saprophytic forms in the                        Perception of Fungal Resources
    seasonally dry forests, was an important                         and Lessons for Integrated Mana-
    finding of those studies and has not been
                                                                     gement
    considered for forest management plans in
    that part of the country.
                                                                           Empirical information is the source
           Further analyses showed that canopy
                                                                     of science and the primary fuel of scienti-
    openness and phosphorus, a forest structu-
                                                                     fic publications. Despite known limitations
    ral variable and a chemical soil parameter,
                                                                     on communicating science (i.e., Gilgun,
    resulted to be the two most important varia-
                                                                     2005; Besley and Tanner, 2011), most re-
    bles explaining the general microclimate of
                                                                     searchers spend quite some time preparing
    the two studied areas. These two variables
                                                                     documents showing their experimentation

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    results. In academic environments, scienti-                      in the Costa Rican population. Even though
    fic publications are still highly regarded al-                   the country is geographically located in the
    though it has been known for decades that                        intermediate anthropological area, the point
    other forms of information exchange are                          of confluence of the mycophilic Mesoame-

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    extremely relevant to translate scientific                       rican region and the mycophobic Chibcha
    content to the non-scientific public (Gar-                       region, few documents have been generated
    vey, 1979). Even today, in the internet era,                     to understand the perceptions of the Costa
    when communication is fast and versatile,                        Rican population towards fungal resources.
    there is a disconnection between the scien-                      This type of non-biological works is highly
    tific community and the public (Fischhoff                        relevant to provide an integrated approach
    and Scheufelec, 2014).                                           to manage fungal resources in the country,
           In Costa Rica, mycological informa-                       along with more standard information on
    tion has been generated for nonprofessionals                     fungal biology.
    in the form of field guides and textbooks                               An ongoing effort in the University of
    (i.e. Mata, 1999; Mata et al., 2003; Calde-                      Costa Rica during the last years has permitted
    rón, 2005; Mata et al., 2010; Mata and Na-                       a basic characterization of the population per-
    varro, 2010; Chaverri et al., 2010, Carranza                     ception on fungi. For example, Molina-Mu-
    et al., 2017). These documents have been                         rillo et al., (2015) studied two groups of peo-
    extremely useful to increase mycoliteracy                        ple in university environments in Honduras

    Figure 1. Temporal canopy differences in seasonally dry and premontane wet forest
    patches of Costa Rica and characteristics of fungal assemblages in them based on Rojas
    and Calvo (2014) and Rojas et al. (2017). Note: the present study is the source for the
    construction of this figure.

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          108
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    (Mesoamerican) and Costa Rica (Interme-                                 Even though some response distribu-
    diate) and attempted to address the reduced                      tions were different between the two coun-
    availability of information at this level in the                 tries, and some differences were found at
    Central American population. The group of                        the gender level, it was interesting to ob-

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    researchers found that the Costa Rican po-                       serve that response associations with video
    pulation was more aware of ecological func-                      games (i.e., Mario Bros), television shows
    tions performed by fungi, but the Honduran                       (i.e., The Smurfs), and world events (i.e.,
    population was more aware of medicinal                           nuclear bomb cloud shape) were recorded
    uses of fungi. Remarkably, for both popu-                        equally in both studied groups. For the ma-
    lations in the 16-35 age group, participants                     jority of the participants surveyed, such as-
    seemed more aware of ecological processes                        pects may be part of their daily life consi-
    than participants in other age groups. More                      dering that cable television and video game
    Costa Ricans (76%) than Hondurans (48%)                          consoles are common among individuals
    responded to have consumed mushrooms in                          attending college worldwide (Jacobsen and
    the month before the survey was conducted.                       Forste, 2011).
    Interestingly, 52% of Hondurans had never                               Results from that study suggested that
    consumed mushrooms versus only 25% of                            exposure to formal education or previous
    Costa Ricans. These results were interes-                        cultural background in the studied groups
    ting considering that Costa Rica was thou-                       may not have played such an important role
    ght to be more mycophobic than Honduras,                         in shaping perceptional views about fungi as
    but they may point to the documented high                        social aspects have. Even though both stu-
    level of self-perceived green mentality in                       died groups have different historical herita-
    Costa Rica that actually represents a double                     ge and levels of emotional proximity with
    discourse in practice (Courvisanos and Jain,                     natural resources, these results showed no
    2006), which may have biased the answers.                        significant differences in their perceptional
           When participants were asked to men-                      patterns toward fungi. As such, it seemed
    tally associate fungi and one aspect of their                    that homogeneity within urban areas due to
    lifestyle, some differences were recorded by                     common globalized stimuli might have pla-
    gender. The most common answers provi-                           yed a more prominent role in determining
    ded by female participants were related to                       natural interactions. This is a very important
    venomous and hallucinogenic aspects of                           argument to consider since the development
    fungal use, whereas males’ answers were                          of management strategies in relation with
    more commonly related to characteristics of                      natural resources should respect particular
    fungi’s edibility and their capacity to be used                  socioeconomic and historical differences.
    as food. Interestingly, responses related to                            For Costa Rica, an unpublished study,
    hallucinogenic uses increased with the age                       carried out with more detail in 11 popula-
    of the participants. When asked about their                      tion centers across the country, also showed
    preference for either animals, plants or fun-                    that regional differences exist within a sma-
    gi, results showed that about 62% of all par-                    ll territory. In this case, when participants
    ticipants mentioned preferring animals and                       were asked if they knew what fungi were,
    about 43% preferred plants, leaving only                         most surveyed people across the country
    5% of answers for fungal preference over                         responded positively, but the lowest percen-
    the other two groups of organisms.                               tages (79% and 76%) of positive responses

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    were found in the only part of Costa Rica                        cations along the dryer Pacific showed the
    with a Mesoamerican cultural background.                         smallest percentages (average of 34% of
    The corresponding area associated with tho-                      answers). At the same time, locations on the
    se responses is located in the lowlands of                       Caribbean coast were associated with the

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    the dry forest region of Costa Rica, which is                    highest percentage of respondents consu-
    similar in biological context to some areas                      ming fungi at least once a month (average of
    of the Mexican state of Oaxaca, but drama-                       41% of answers), and respondents in towns
    tically different in the social perception on                    located on the Pacific side of Costa Rica
    fungi, for example. Such type of differen-                       showed the lowest values of monthly fungal
    ces has been documented, however, around                         consumption (average of 32% of answers).
    deep social issues within mycophilic re-                         The significant correlation between repor-
    gions, between low and high elevation areas,                     ted consumption of fungi and perceptional
    with different forest ecosystems as well (see                    value of fungi as a source of food was mo-
    Thompson 1970). Similarly, when partici-                         derately high (r=0.71), suggesting that, in
    pants were asked if fungi were important for                     this particular aspect, the Costa Rican so-
    ecosystem functions, a vast majority answe-                      ciety might have learned the value of fungi
    red positively. However, communities loca-                       as a source of food by ingesting the source
    ted along the north and central Pacific coast,                   itself. The latter seems to be more prevalent
    where seasonally dry forests occur, showed                       in population centers with wet and rain fo-
    the lowest percentages of positive respon-                       rests than in those with dry forests.
    ses (63% in average versus 82% for highly                                The examples provided herein are
    educated communities in the center of the                        simple demonstrations that surveys could
    country). Ironically, when participants were                     be useful to determine guidelines for na-
    given four real ecological roles of fungi in                     tural resource management (see Brown,
    forests, 45% failed to recognize at least two                    2004) and public interaction with fungi.
    of those roles, and the largest percentage of                    In the case of this group of organisms, this
    participants correctly associating three or                      exercise has been conducted in Costa Rica
    four roles (33% in average) were found in                        for the first time in recent years, and the
    highly educated regions. Despite the latter,                     complete analyses have not been published
    no correlations were found between the hu-                       yet. However, some of the information con-
    man development index of the population                          tained in these public opinion assessments
    centers and the answer distribution found in                     is important to understand sociocultural,
    the study, suggesting that responses have a                      economic, and historical links of particular
    cultural background more than a socioeco-                        sectors of the population with a number of
    nomic one.                                                       natural resources. Such a task of understa-
           When participants were asked about                        ding the human-nature interaction is easier
    the most important use of fungi for human                        to implement for widely valued resources
    lifestyles, their value as a source of food and                  such as water and air (Bergstrom and Ran-
    medicines was provided by 44% and 23%                            dall, 2016), and harder for poorly known
    of all participants. Interestingly, Caribbean                    biological groups such as the fungi. Howe-
    centers with tropical rainforest showed the                      ver, those constraints have shown that in the
    highest values (an average of 55% of all                         Costa Rican case, there are opportunities of
    answers in their respective town), and lo-                       mycoliteracy in most areas of the country

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          110
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    and formal biological research could also be                     be missed these days. For instance, from a
    reinterpreted to reach those populations (see                    series of informative videos produced by
    Stone, 2017).                                                    the authors of this chapter and uploaded to a
                                                                     popular online platform, one specific video

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    Lessons from Fungal Research in                                  on the biology of Amanita muscaria sen-
    the Context of Development and                                   su lato has received 100 times more visits
                                                                     (between 2014 and 2017) than other 30 vi-
    Conservation of Natural Resources
                                                                     deos produced on other topics. In the end,
                                                                     the importance of active research in a field
          In 2011, Costa Rica held the Latin
                                                                     of study for the development of local socie-
    American Mycological Congress organized
                                                                     ties, as mentioned earlier, is the translation
    by the Latin American Mycological Asso-
                                                                     of scientific information into products that
    ciation. This is the most important interna-
                                                                     those societies can use for purposes ranging
    tional event on mycology in the region, and
                                                                     in all disciplines of human knowledge.
    it was an accomplishment to organize such
                                                                            For Costa Rica, this translation of
    event in this country at that time. An execu-
                                                                     active research into tangible products, pu-
    tive decree from the President of Costa Rica
                                                                     blicly available online, seems to have been
    declared this an event of public interest (De-
                                                                     successful in the last years. As a proxy to
    creto ejecutivo 36573-MICIT, 2011). Such
                                                                     evaluate such availability of information,
    meeting was possible thanks to academic
                                                                     when a search (in Spanish) was performed
    and government support, a critical number
                                                                     on Google Scholar looking for resources
    of internal researchers working on myco-
                                                                     dealing with fungi in association with the
    logical issues, and the fact that, within the
                                                                     different countries in Central America and
    Mesoamerican biodiversity region, Costa
                                                                     Mexico, it was evident that Costa Rica had
    Rica was recognized as one of the growing
                                                                     carried out this work more efficiently than
    centers of fungal studies. The most impor-
                                                                     the average for the other regional countries
    tant aspect brought into the country by this
                                                                     (Figure 2). As a comparison, Mexico is very
    event, however, was the promotion of my-
                                                                     rich in fungal resources and human-fungi
    cology among the younger generation of
                                                                     interactions, and mycological studies are
    Costa Ricans that had not been exposed to
                                                                     usually more publicized than in other parts
    the topic.
                                                                     of Latin America due to the mycophilic
          This exposure to fungi during the 21st
                                                                     character of the Mexican population. Even
    century, particularly with online resources,
                                                                     though there are obvious limitations to the
    should be carried out with multimodal te-
                                                                     analysis of results from this type of public
    chniques (see Jewitt, 2012). The availability
                                                                     platforms on the internet, they can also pro-
    of information on the internet is an impor-
                                                                     vide interesting data for comparison purpo-
    tant aspect to consider in the development
                                                                     ses with more professional and specialized
    of longterm scientific programs, given the
                                                                     databases (Falagas et al., 2008). However,
    increased dependence on internet resources
                                                                     in the end, the availability of fungal informa-
    (Sheenan and Young, 2012). The advanta-
                                                                     tion in public and easy-to-use platforms has a
    ge of fungi is that they are appealing and
                                                                     higher potential of reaching non-specialized
    interesting for many people, and the oppor-
                                                                     public (non-mycologists), and it is very im-
    tunity to develop these multimodal approa-
                                                                     portant for educational purposes.
    ches to communicate mycology should not

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          111
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           Despite the latter, someone still must                    the use and value of regional fungi by auto-
    generate such information and resour-                            chthonous populations.
    ces and it seems that established groups                                Using information from the Universi-
    (professional and non-professional) are                          ty of Costa Rica´s Research Office, which

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    more productive for the communication of                         records thematic research in Costa Rica sin-
    science, including mycology, when they                           ce 1975 (www.vinv.ucr.ac.cr), it seems clear
    become the active participants of the pro-                       that fungal studies in this country, during
    cess (see Pagani and Malacarne, 2017).                           the last 40 years, have not been designed to
    However, for these approaches to take pla-                       reach the public. For example, only 15% of
    ce effectively, in an equilibrated manner,                       proposed projects on fungi have had a social
    non-professional groups should also exist                        application component and none of the pro-
    to counterbalance the academic-based                             jects during that time have included citizen
    (and academically-biased) delivery of in-                        science promotion of some kind. As such,
    formation from fungal researchers. In this                       the connectivity between mycology and the
    sense, the promotion of mycology should                          triple helix, a socioeconomic approach pro-
    reach all strata of societies with differential                  posed for developing countries that seeks
    approaches, so collective efforts compen-                        to link academia, productive sector and go-
    sate specific biases.                                            vernments (see Molina-Murillo and Rojas,
           In Costa Rica, one limitation of this                     2015), has been very limited in Costa Rica.
    active process of mycological communica-                                Overall, mycology in Costa Rica has
    tion has been the reserved role of nonpro-                       focused on the primary basic biological
    fessionals and the reduced promotion of                          aspects. In this sense, local and foreign
    citizen science for the generation of infor-                     researchers in the country have generated
    mation. These two types of contribution are                      important information to understand taxo-
    acknowledged to be important factors pro-                        nomic and distributional patterns of fungi.
    moting science in societies (Bonney et al.,                      Even though fungal studies in the coun-
    2014; Bonney et al., 2015). Even though                          try have had a multidisciplinary approach
    the field guides on fungi produced by the                        in the present century, they still lack real
    National Institute of Biodiversity (INBio)                       applicability and connectivity with Costa
    (Mata, 1999; Mata et al., 2003, Chaverri et                      Rica´s development strategy. However, in
    al., 2010), and several websites produced in                     terms of fungal conservation and adminis-
    recent decades have been important contri-                       tration of fungal resources, this country
    butors to disseminate information on fungi                       has established a series of public measu-
    in the country, public empowerment and                           rements to include fungi in non-academic
    “ownership” of mycological information by                        agendas. The latter has positioned Costa
    nonprofessionals have not been well stimu-                       Rica slightly ahead of other countries in
    lated in this territory. Unfortunately, public                   the same region in terms of integrating fun-
    offices in charge of natural resources (inclu-                   gi in the management of nature. For this and
    ding fungi) integration with social stakehol-                    other initiatives, from a global perspective
    ders have placed their interest in the disse-                    including other taxonomic groups, Costa
    mination of information on the cultivation                       Rica has been used as a case study in Latin
    of introduced fungal species rather than on                      America (Zimmerer, 2011).
    the rescue of local knowledge in relation to

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          112
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    Figure 2. Availability of results in response to a search for fungi in Google Scholar
    during the period 1990-2017 for Mexico, Costa Rica and the average of Central American
    countries excluding Costa Rica. All trend lines are shown and correspond to quadratic
    functions with parametric correlation values higher than 0.90. Note: the present study is the

                                                                                                                                  UNICIENCIA Vol. 33, N°. 1, pp. 101-117. Enero-Junio, 2019 • URL: www.revistas.una.ac.cr/uniciencia • Correo electrónico: revistauniciencia@una.cr
    source for the construction of this figure.

           Recent ecological studies carried out                     food or as part of industrial applications could
    in the country have generated important in-                      be interesting to identify in Costa Rica for the
    formation to understand fungal dynamics in                       development of future applications. Interes-
    the context of ecosystem services and climate                    tingly, the issues exposed herein, focused on
    change. Also, opinion studies carried out in                     the Costa Rican case, are examples of simi-
    Costa Rica have been useful to analyze so-                       lar matters taking place in other parts of the
    cioeconomic, cultural, and gender-based per-                     world. Hopefully, shared lessons can lead to
    ceptional views in the different regions of the                  important accomplishments beyond political
    country. The interaction of these two research                   borders for the benefit of everyone someday.
    lines is imperative for an effective and mo-
    dern approach to manage fungal resources in                      Acknowledgements
    such territory. However, inequalities in my-
    coliteracy across Costa Rica should be ad-                              We would like to extend our gratitude
    dressed with multiapproach channels, among                       to Pedro Rojas and Sergio Molina-Murillo for
    which the internet is prominent. With a future                   their help collecting some of the data used in
    promotion of citizen science-based research                      this review. The field work that generated the
    and community-based projects involving fun-                      information presented herein was funded by
    gi, maybe social proximity to this group of                      projects 731-B2-222, 731-B4-249, and 731-
    organisms would allow more effective inte-                       B5-059 from Vicerrectoría de Investigación
    raction with them. Potential entrepreneurs se-                   at the University of Costa Rica.
    tting up initiatives using fungi as a source of

Carlos Rojas-Alvarado y Randall Valverde- González                                                                          113
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Carlos Rojas-Alvarado y Randall Valverde- González                                                                          115
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