Abstract:
Information on distribution, number of populations, and biotic interactions are essential for assessing the threat status of species and to establish more effective conservation initiatives. Ecological niche modeling have been successfully applied to identify the potential distribution, even for rare species that have few recorded occurrence points. In this study, we evaluated the potential distribution and additionally generated the first data on the reproductive biology of Discocactus ferricola, due to its degree of threat and the absence of ecological data for that species. The potential distribution map highlighted areas with higher probability of occurrence of D. ferricola on the Residual Plateau of Maciço do Urucum located in Mato Grosso do Sul, Brazil. The occurrence of D. ferricola populations was limited to outcrops of flat ironstone (cangas) distributed in patches across the landscape, increasing the chances of serious threats, such as habitat loss due to mining and species extraction. We also found that D. ferricola is xenogamous. Therefore, in situ conservation actions must prioritize the maintenance of interactions with pollinators by preserving the flora and fauna of rocky outcrops and adjacent forests in areas of greater environmental suitability for D. ferricola. Our study highlights the use of ecological niche modeling and data on biotic interactions to evaluate species potential distribution, to guide new sampling efforts, and to assist conservation and management initiatives.
Keywords:
Conservation; ecological niche modeling; pollinator dependence; outcrop; restrict distribution
Resumo:
Informações sobre distribuição, número de populações e interações bióticas são essenciais para avaliar o status de ameaça das espécies e estabelecer iniciativas de conservação mais eficazes. A modelagem de nicho ecológico tem sido aplicada com sucesso para identificar a distribuição potencial, mesmo para espécies raras que possuem poucos pontos de ocorrência registrados. Neste estudo, avaliamos a distribuição potencial e adicionalmente geramos os primeiros dados sobre a biologia reprodutiva de Discocactus ferricola, devido ao seu grau de ameaça e à ausência de dados ecológicos para essa espécie. O mapa de distribuição potencial destacou áreas com maior probabilidade de ocorrência de D. ferricola no Planalto Residual do Maciço do Urucum localizado em Mato Grosso do Sul, Brasil. A ocorrência de populações de D. ferricola foi limitada aos afloramentos ferruginosos planos (cangas) que são distribuídos em manchas pela paisagem, aumentando as chances de ameaças graves, como perda de habitat devido à mineração e extração da espécie. Também descobrimos que D. ferricola é xenogâmica. Portanto, ações de conservação in situ devem priorizar a manutenção das interações com os polinizadores através da preservação da flora e da fauna nos afloramentos rochosos e florestas adjacentes nas áreas de maior adequabilidade ambiental para D. ferricola. Nesse estudo, nós destacamos o uso da modelagem de nicho ecológico e de dados sobre interações bióticas para avaliar a distribuição potencial de espécies, orientar novos esforços de amostragem e auxiliar iniciativas de conservação e manejo.
Palavras-chave:
afloramentos rochosos; conservação; dependência de polinizador; distribuição restrita; modelagem de nicho ecológico
Introduction
The occurrence points of a species carry information about its distribution, which is a complex expression of its ecology and evolutionary history (Brown 1995BROWN, J.H. 1995. Macroecology. University of Chicago Press, Chicago.). Each point reflects part of realized niche and, therefore, contains information on abiotic conditions, biotic interactions, and the dispersion capacity that are required for the occurrence of species (Soberón & Peterson 2005SOBERÓN, J. & PETERSON, A.T. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers. Inform. 2:1-10.). Thus, the points of occurrence can be used to construct ecological niche models (ENM) also known as species distribution models (SDM) (Soberón & Peterson 2005SOBERÓN, J. & PETERSON, A.T. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers. Inform. 2:1-10., Peterson et al. 2011PETERSON, A. T., SOBERÓN, J., PEARSON, R. G., ANDERSON, R. P., MARTÍNEZ-MEYER, E., NAKAMURA, M. & ARAÚJO, M. B. 2011. Ecological niches and geographic distributions. Princeton University Press, Princeton., Peterson & Soberón 2012PETERSON, A.T. & SOBERÓN, J. 2012. Species distribution modeling and ecological niche modeling: getting the concepts right. Nat. Conservação 10(2):1-6.). This approach is considered of low cost and has been applied to several researches, especially for the conservation of species and biomes (Le Lay et al. 2010LE LAY, G., ENGLER, R., FRANC, E. & GUISAN, A. 2010. Prospective sampling based on model ensembles improves the detection of rare species. Ecography 33(6):1015-1027., Werneck et al. 2012WERNECK, F.P., NOGUEIRA, C., COLLI, G.R., SITES JUNIOR J.W. & COSTA, G.C. 2012. Climatic stability in the Brazilian Cerrado: implications for biogeographical connections of South American savannas, species richness and conservation in a biodiversity hotspot. J. Biogeogr. 39(9):1695-706., Sobral-Souza et al. 2018SOBRAL-SOUZA, T., VANCINE, M.H., RIBEIRO, M.C. & LIMA-RIBEIRO, M.S. 2018. Efficiency of protected areas in Amazon and Atlantic Forest conservation: A spatio-temporal view. Acta Oecol. 87:1-7., Adhikari et al. 2019ADHIKARI, D., TIWARY, R., SINGH, P.P., UPADHAYA, K., SINGH, B., HARIDASAN, K.E., BHATT, B.B., CHETTRI, A. & BARIK, S.K. 2019. Ecological niche modeling as a cumulative environmental impact assessment tool for biodiversity assessment and conservation planning: A case study of critically endangered plant Lagerstroemia minuticarpa in the Indian Eastern Himalaya. J. Environ. Manage. 243:299-307., Kolanowska & Jakubska-Busse 2020KOLANOWSKA, M. & JAKUBSKA-BUSSE, A. 2020. Is the lady’s-slipper orchid (Cypripedium calceolus) likely to shortly become extinct in Europe?-Insights based on ecological niche modelling. PLoS One 15(1):e0228420.). Specifically, ENM has been used to identify likely areas for invasive species (Qiao et al. 2017QIAO, H., ESCOBAR, L.E. & PETERSON, A.T. 2017. Accessible areas in ecological niche comparisons of invasive species: Recognized but still overlooked. Sci. Rep-Uk 7(1):1-9., Zhu et al. 2017ZHU, J., XU, X., TAO, Q., YI, P., YU, D. & XU, X. 2017. High invasion potential of Hydrilla verticillata in the Americas predicted using ecological niche modeling combined with genetic data. Ecol. Evol. 7(13):4982-4990.), in paleoecological studies (Lima-Ribeiro & Diniz-Filho 2013LIMA-RIBEIRO, M.S. & DINIZ-FILHO, J.A.F. 2013. Modelos ecológicos e a extinção da megafauna: clima e homem na América do Sul. Cubo, São Carlos.), to highlight areas of potential distribution (McCune 2016MCCUNE, J.L. 2016. Species distribution models predict rare species occurrences despite significant effects of landscape context. J. Appl. Ecol. 53(6):1871-1879., Fois et al. 2018FOIS, M., CUENA-LOMBRAÑA, A., FENU, G. & BACCHETTA, G. 2018. Using species distribution models at local scale to guide the search of poorly known species: Review, methodological issues and future directions. Ecol. Model. 385:124-132.), to indicate areas for species reintroduction (Martínez-Meyer et al. 2006MARTINEZ-MEYER, E., PETERSON, A.T., SERVÍN, J.I. & KIFF, L.F. 2006. Ecological niche modelling and prioritizing areas for species reintroductions. Oryx 40(4):411-418.), among others.
Noteworthy, ecological niche modeling have been successfully applied to provide information on potential distribution of species even with few recorded occurrence points (Le Lay et al. 2010LE LAY, G., ENGLER, R., FRANC, E. & GUISAN, A. 2010. Prospective sampling based on model ensembles improves the detection of rare species. Ecography 33(6):1015-1027., McCune 2016MCCUNE, J.L. 2016. Species distribution models predict rare species occurrences despite significant effects of landscape context. J. Appl. Ecol. 53(6):1871-1879., Fois et al. 2018FOIS, M., CUENA-LOMBRAÑA, A., FENU, G. & BACCHETTA, G. 2018. Using species distribution models at local scale to guide the search of poorly known species: Review, methodological issues and future directions. Ecol. Model. 385:124-132.). Distribution data is important for the assessment of the threat status of these species, since the extent of occurrence and number of populations are criteria used to define threat categories of the International Union for Conservation of Nature (IUCN) (Martinelli & Moraes 2013MARTINELLI, G. & MORAES, M.A. 2013. Livro vermelho da flora do Brasil. Instituto de Pesquisas Jardim Botânico do Rio de Janeiro, Rio de Janeiro.). After identifying the threat level, the next step is to implement in situ and or ex situ management actions, when necessary. For the correct management of species, information about their ecology, including reproductive aspects and biotic interactions, are required (Scheele et al. 2018SCHEELE, B.C., LEGGE, S., ARMSTRONG, D.P., COPLEY, P., ROBINSON, N., SOUTHWELL, D., WESTGATE M.J. & LINDENMAYER D.B. 2018. How to improve threatened species management: an Australian perspective. J. Environ. Manage. 223:668-675.). The lack of these information weaken management and conservation strategies, prevent adequate actions for population growth, and obscure the construction of more assertive hypotheses about the evolution and dispersion of species.
Basic information on distribution and reproductive biology are crucial for assessments of the current threat status of species and for the establishment of more accurate conservation plans, especially for rare and endangered species such as Discocactus ferricola Buining & Brederoo (Machado 2004MACHADO, M.C. 2004. O gênero Discocactus Pfeiff. (Cactaceae) no estado da Bahia, Brasil: variabilidade morfológica, variabilidade genética, taxonomia e conservação. MSc Thesis, Universidade Estadual de Feira de Santana, Feira de Santana. PPGBot. http://www.ppgbot.uefs.br (last access in 04/07/2020).
http://www.ppgbot.uefs.br...
, Ribeiro-Silva et al. 2011RIBEIRO-SILVA, S., ZAPPI, D.C., TAYLOR, N.P. & MACHADO, M.C. 2011. Plano de Ação Nacional para a conservação das Cactáceas. Série Espécies Ameaçadas nº 24. Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do Meio Ambiente, Brasília.). This species is currently categorized as endangered on the Red List of Threatened Species of IUCN, mainly due to its small area of occurrence and small number of known populations (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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). In this study, we used the ecological niche modeling approach to assess the potential distribution and additionally to generate the first ecological data on reproductive biology of D. ferricola. The general aim of this study was to provide ecological data of D. ferricola to assist in conservation initiatives and to guide new sampling efforts. Specifically, we aimed to answer the following questions: (1) What is the current potential distribution of D. ferricola? (2) Does D. ferricola depend on pollinators for reproduction? (3) What species visit D. ferricola flowers?
Material and Methods
1. Study area
The present study was carried out on eight farms, a settlement and a municipal park, all located in the mountainous complex of the Residual Plateau of Maciço do Urucum (RPMU), in the municipalities of Corumbá and Ladário in Mato Grosso do Sul state, MS, Brazil (Tab. 1). According to Köppen’s classification, the climate of the region is Aw megathermal, with dry winters and rainy summers (Soriano 2000SORIANO, B.M.A. 2000. Climatologia. In Zoneamento ambiental da Borda Oeste do Pantanal: Maciço do Urucum e Adjacências (J.S.V. Silva ed.). Embrapa, Brasília, p. 69-82.). The average annual temperature is 25.1°C, with maximum temperatures reaching 40°C and minimum temperatures close to 0°C (Soriano 2000SORIANO, B.M.A. 2000. Climatologia. In Zoneamento ambiental da Borda Oeste do Pantanal: Maciço do Urucum e Adjacências (J.S.V. Silva ed.). Embrapa, Brasília, p. 69-82.). The average annual precipitation is 1070 mm, and the average annual relative humidity is 75% (Soriano 2000SORIANO, B.M.A. 2000. Climatologia. In Zoneamento ambiental da Borda Oeste do Pantanal: Maciço do Urucum e Adjacências (J.S.V. Silva ed.). Embrapa, Brasília, p. 69-82.).
Occurrence sites of Discocactus ferricola on the Residual Plateau of Maciço do Urucum, Mato Grosso do Sul state, Brazil.
2. Studied species
Discocactus ferricola has a flattened globular shape with a pale to dark green stem measuring 8-9 cm high and 20-25 cm in diameter (Anderson 2001ANDERSON, E.F. 2001. The cactus family. Timber Press, Portland.). The number of ribs is 14, and they form tubercles (Anderson 2001). The 5-8 spines, arranged radially, are 4.5-5 cm and brown, becoming gray with age. The central spines are mostly absent but may present as one spine at 2-2.5 cm (Anderson 2001ANDERSON, E.F. 2001. The cactus family. Timber Press, Portland.). The cephalium measures 7 cm high and 6.5 cm in diameter and has white wool with dark gray bristles that can be 5 cm (Anderson 2001ANDERSON, E.F. 2001. The cactus family. Timber Press, Portland.). The flowers are white and tubular and measure 5.5 cm long (Figure 1A). The fruits are elongate to club shaped, measure 3-4 cm long, and are greenish cream to white. Seeds are broadly oval to subglobose and are shiny black color, with numerous papillae or tubercles, and they measure 2-2.5 mm long (Anderson 2001ANDERSON, E.F. 2001. The cactus family. Timber Press, Portland.).
Discocactus ferricola. A. A closer look at one individual with opened nocturnal flowers. B. Flat ironstone outcrop area on the Vale do Paraíso farm showing the locally abundant population of D. ferricola. The arrows show aggregate individuals forming large clumps. The reddish color of the soil is typical of ironstone outcrops.
Discocactus ferricola is endemic to the mountainous complex of the RPMU on the border of Brazil and Bolivia (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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, Takahasi & Meirelles 2014TAKAHASI, A. & MEIRELLES, S.T. 2014. Ecologia da vegetação herbácea de bancadas lateríticas (cangas) em Corumbá, MS, Brasil. Hoehnea 41(4):515-528.). The RPMU is known as the oldest rock formation in the world, with intact exposed rocks that are approximately 70 million years old (Vasconcelos et al. 2019VASCONCELOS, P.M., FARLEY, K.A., STONE, J., PIACENTINI, T. & FIFIELD, L.K. 2019. Stranded landscapes in the humid tropics: Earth’s oldest land surfaces. Earth Planetary Sc. Let. 519:152-164.). In the RPMU, D. ferricola occurs on flat ironstone outcrops, locally known as “bancadas lateríticas” or “cangas”, formed by the deposition of iron and manganese laterites in the drainage areas of the hills and slopes (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
https://dx.doi.org/10.2305/IUCN.UK.2013-...
, Takahasi & Meirelles 2014TAKAHASI, A. & MEIRELLES, S.T. 2014. Ecologia da vegetação herbácea de bancadas lateríticas (cangas) em Corumbá, MS, Brasil. Hoehnea 41(4):515-528.). Discocactus ferricola have clonal reproduction and is abundant locally, forming large aggregates (Figure 1B).
Currently, the main threats to D. ferricola are habitat loss due to mining (especially in Bolivia), human occupation, and species extraction, as this species is consumed as food, used as herbal medicine by traditional communities, and has ornamental potential (Lüthy 2001LÜTHY, J.M. 2001. CITES identification manual: The cacti of CITES appendix I. CITES, Federal Veterinary Office Switzerland, Botanical Garden of the University of Berne, IOS & Sukulent-Sammlung Zürich, Bern. , Ribeiro-Silva et al. 2011RIBEIRO-SILVA, S., ZAPPI, D.C., TAYLOR, N.P. & MACHADO, M.C. 2011. Plano de Ação Nacional para a conservação das Cactáceas. Série Espécies Ameaçadas nº 24. Instituto Chico Mendes de Conservação da Biodiversidade, Ministério do Meio Ambiente, Brasília., Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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). The total area of occurrence of D. ferricola is approximately 20 km2 patchily distributed on three outcrops of iron ore and manganese surrounded by Cerrado vegetation and forests (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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). Such habitats are threatened by mining and urbanization, which has led to a 30% population decline of D. ferricola over the last 30 years (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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). The continuous loss of adult individuals, its occurrence out of protected areas, and its generation time of 10 years also justify the endangered status of D. ferricola (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
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).
3. Species distribution modeling
To identify areas of greatest climatic suitability for D. ferricola, we initially performed a search on the Global Biodiversity Information Facility (GBIF) and Species Link platforms to access all recorded occurrences. In addition, we actively searched for D. ferricola populations in the RPMU. The occurrence points were used to construct D. ferricola occurrence map. After removing uncertain, redundant, and historical data, we had 11 occurrence points of D. ferricola covering the entire known distribution of the species (Tab. 1). To remove environmentally autocorrelated points, a rarefaction analysis for environmental heterogeneity was carried out in ArcGIS v.10.3 (Anderson & Gonzalez 2011ANDERSON, R.P. & GONZALEZ, J.I. 2011. Species-specific tuning increases robustness to sampling bias in models of species distributions: an implementation with Maxent. Ecol. Model. 222(15):2796-2811., ESRI 2014ESRI. 2014. ArcGIS Desktop: Release 10.3. Environmental Systems Research Institute, Redlands., Varela et al. 2014VARELA, S., ANDERSON, R.P., GARCÍA-VALDÉS, R. & FERNÁNDEZ-GONZÁLEZ, F. 2014. Environmental filters reduce the effects of sampling bias and improve predictions of ecological niche models. Ecography 37(11):1084-1091.). The remaining 10 occurrence points were used to model the potential niche of the species (Tab. 1). The area included in the model extended approximately 140000 km2 and contained the main rock outcrops of the region: 1- Rincon del Tigre in Bolivia, 2 - Serra do Amolar, 3 - Residual Plateau of Maciço do Urucum, and 4 - Serra da Bodoquena in Brazil.
We used bioclimatic variables from the WorldClim database at a resolution of 30 arc sec (~1 km2) (www.worldclim.org, Fick & Hijmans 2017FICK, S.E. & HIJMANS, R.J. 2017. Worldclim 2: New 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37(12):4302-4315.) and the maximum entropy algorithm (MaxEnt v.3.4.1, Phillips et al. 2006PHILLIPS, S.J., ANDERSON, R.P., & SCHAPIRE, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190(3-4):231-259.) to model the potential niche distribution of D. ferricola. We used the area under the curve (AUC) receiver operating characteristics (ROC) to validate the output model from MaxEnt. We then used the maximum threshold value to produce a binary map and True Skill Statistics to evaluate its reliability (Allouche et al. 2006ALLOUCHE, O., TSOAR, A. & KADMON, R. 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43(6):1223-1232.). Thus, we generated a final map that narrowed the searches for new populations in areas where D. ferricola would most likely occur. Four variables were used in the modeling: mean diurnal range (BIO2, mean monthly temperature (max temp - min temp)), mean temperature of the warmest quarter (BIO10), annual precipitation (BIO12), and precipitation of driest quarter (BIO17). The four variables were selected after a principal axis factor analysis with varimax rotation in a data set consisting of 19 bioclimatic variables, an elevation raster available from the database USGS (hydrosheds.cr.usgs.gov), and the Harmonized World Soil raster (www.fao.org, Fischer et al. 2008FISCHER, G., NACHTERGAELE, F., PRIELER, S., VAN VELTHUIZEN, H. T., VERELST, L. & WIBERG, D. 2008. Global Agro-ecological Zones Assessment for Agriculture (GAEZ 2008). IIASA Austria and Rome, FAO, Laxenburg.). We conducted analyses in R v.3.5.2 (R Core Team 2018R CORE TEAM. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/.
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) using the packages “vegan” (Oksanen et al. 2018OKSANEN, J., BLANCHET, F.G., FRIENDLY, M., KINDT, R., LEGENDRE, P., MCGLINN, D., MINCHIN, P. R., O’HARA, R.B., SIMPSON, G. L, SOLYMOS, P., STEVENS, M. H.H., SZOECS, E. & WAGNER, H. 2018. Vegan: Community Ecology Package. R package version 2.5-3. https://CRAN.R-project.org/package=vegan
https://CRAN.R-project.org/package=vegan...
), “raster” (Hijmans 2018HIJMANS, R.J. 2018. Raster: Geographic Data Analysis and Modeling. R package version 2.8-4. https://CRAN.R-project.org/package=raster
https://CRAN.R-project.org/package=raste...
), and “rgdal” (Nenzén & Araújo 2011NENZÉN, H.K. & ARAÚJO, M.B. 2011. Choice of threshold alters projections of species range shifts under climate change. Ecol. Model. 222(18):3346-3354., Porfirio et al. 2014PORFIRIO, L.L., HARRIS, R.M., LEFROY, E.C., HUGH, S., GOULD, S.F., LEE, G., BINDOFF, N.L. & MACKEY, B. 2014. Improving the use of species distribution models in conservation planning and management under climate change. PLoS One 9(11):e113749., Bivand et al. 2018BIVAND, R., KEITT, T. & ROWLINGSON, B. 2018. rgdal: Bindings for the ‘Geospatial’ Data Abstraction Library. R package version 1.3-6. https://CRAN.R-project.org/package=rgdal
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).
4. Pollinator dependence
We conducted four treatments on 46 flowers from 25 individuals to determine if D. ferricola depends on a pollinator for reproduction: (1) unmanipulated self-pollination (n = nine flowers) - the intact flower buds were bagged, and there was no additional manipulation; (2) manual self-pollination (n = 10 flowers) - intact flower buds were bagged, and as soon as the flowers opened, they were manually pollinated with their own pollen; (3) manual cross-pollination (n = 13 flowers) - intact flower buds were bagged, and as soon as the flowers opened, they were emasculated and pollinated with pollen grains from different individuals; and (4) natural pollination (n = 14 flowers) - flowers accessible to pollinators were marked as a control. Treatments were conducted on individuals from Vale do Paraíso Farm from November 2017 to February 2018.
We used generalized linear models (GLMs) with binomial and Poisson distributions to look for treatment effects regarding the probabilities of fruit formation and number of seeds per fruit, respectively. We determined overdispersion and model fit through residual analyses (Zuur et al. 2007ZUUR, A.F., IENO, E.N. & SMITH, G.M. 2007. Analysing Ecological Data. Springer Science + Business Media, New York., Mazerolle 2019MAZEROLLE, M.J. 2019. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package.). Because we found overdispersion in the GLM with a Poisson distribution, standard errors were corrected using the dispersion parameter in a quasi-GLM. We formulated two competitive models for each response variable (Tab. 2). We fitted models to the data and ranked them according to Akaike’s information criterion with a second-order bias adjustment (AICc, Burnham & Anderson 2002BURNHAM, K.P. & ANDERSON, DR. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2 ed. Springer Science + Business Media, New York., Anderson 2008ANDERSON, D.R. 2008. Model Based Inference in the Life Sciences: a Primer on Evidence. Springer Science + Business Media, New York.). We used ΔAICc, the 95% confidence interval of the regressor, Akaike’s weights (AICcW), and the evidence ratio to compare the competitive models (Burnham & Anderson 2002BURNHAM, K.P. & ANDERSON, DR. 2002. Model selection and multimodel inference: a practical information-theoretic approach. 2 ed. Springer Science + Business Media, New York., Anderson 2008ANDERSON, D.R. 2008. Model Based Inference in the Life Sciences: a Primer on Evidence. Springer Science + Business Media, New York.). We conducted analyses in R 3.5.2 (R Development Core Team) using the packages AICcmodavg (Mazerolle 2019MAZEROLLE, M.J. 2019. AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). R package.), binom (Dorai-Raj 2015DORAI-RAJ, S. 2015. binom: binomial confidence intervals for several parameterizations. R package.), bbmle (Bolker et al. 2020BOLKER, B., R DEVELOPMENT CORE TEAM & GINÉ-VÁZQUES, I. 2020. bbmle: tools for general Maximum likelihood estimation. R package.), and stats (Bolar 2019BOLAR, K. 2019. STAT: interactive document for working with basic statistical analysis. R package.).
Model selection table for the probability of fruit formation and number of seeds per fruit in Discocactus ferricola for different reproduction treatments: natural pollination and manual cross-pollination. K: number of parameters; AICc: Akaike’s information criterion with the second bias adjustment; AICcW: AICc weighted; b ± se: estimated beta ± standard deviations; 95% CI: 95% confidence interval for beta; ER: evidence ratio; ~ 1 (constant): model representing no differences between treatments; ~ Treatments: model representing the hypothesis of a treatment effect.
5. Floral visitors
We recorded floral visitors during field observations in the mornings (7 h-10 h; n = four days), afternoons (15 h-18 h; n = three days), and evenings (18 h-21 h; n = three days) for two populations: Vale do Paraíso and São João farms. We categorized species as floral visitors if they touched the reproductive parts of the flowers. Floral visitors were photographed and, whenever possible, were collected, preserved in 70% alcohol, and sent to specialists for identification. We also used a camera trap (Reconyx©) to record nocturnal pollinators. The camera was placed in two different locations on the Vale do Paraíso Farm for six days, totaling 144 hours of sampling effort.
Results
1. Species distribution modeling
We generated a map that shows areas of high climatic suitability for D. ferricola based on niche modeling through the maximum entropy algorithm (AUC = 0.97; Figure 2). The TSS on the maximum threshold indicated a good fit of the final model (TSS = 0.67). The model indicated areas with adequate climates for the occurrence of D. ferricola in small discontinuous areas of the Serra do Amolar and on some nearby hills, as well as in the Serra da Bodoquena (Figure 2A-B). However, the greatest areas of climatic suitability for D. ferricola were concentrated on the hills of RPMU, specifically on the Urucum, Grande, Rabichão, São Domingos, and Mutum hills (Figure 2B).
Geographic distribution of Discocactus ferricola populations. A. Elevation map of the area used in the modeling (background), showing the rocky outcrops of the region. B. Map of climatic suitability for D. ferricola.
2. Pollinator dependence
Only the manual cross pollination and natural pollination treatments produced fruits and, therefore, were included in the statistical analyses. The mean probability of fruit formation for natural pollination was 57% (95% CI = 33% - 79%; n = 14 flowers resulting in eight fruits), while for manual cross pollination, it was 85% (95% CI = 57% - 87%; n = 13 flowers resulting in 11 fruits). Although the estimated probability of fruit formation varied according to treatments, our data did not allow us to distinguish between the null and the alternative hypothesis of a treatment effect. That result was clear from the small values of ΔAICc (< 2.0) and the evidence ratio being close to one (Tab. 2). Regarding the number of seeds produced per fruit, our data strongly supported the hypothesis that there were more seeds in fruits that were manually pollinized. Such a result was confirmed by the large ΔAICc of the constant model (>> 7.00) and the AICcW for the treatments model (Tab. 2). The estimated mean number of seeds per fruit through manual pollination was 43 (95% IC = 36 - 52; n = 11), which was 2.4 times the estimated mean number of 18 seeds produced per fruit through natural pollination (95% IC = 14 - 23; n = 8).
3. Floral visitors
During the mornings, we found small beetles from the Nitidulidae family covered in pollen inside closed flowers of D. ferricola, which had been open the night before (Figure 3A). During the afternoons, we observed that as soon as the flower buds of D. ferricola emerged from the cephalium, small beetles from the Nitidulidae family pierced and penetrated them (Figure 3B). Discocactus ferricola flowers opened at approximately 6 p.m. (n = seven days) and closed at approximately 2 a.m. (n = five days). During the nocturnal observations, we found the same beetle species as those observed during the mornings visiting opened flowers (Figure 3C). Moreover, we found larvae of the beetles on older flowers, i.e., those that had closed on the previous days. Other species of beetles belonging to the Chrysomelidae family were found visiting the flowers and mating inside them at night (Figure 3D). Finally, using camera traps, we recorded visits of moths to the D. ferricola flowers. We registered four moth visits between 7 p.m. and 1 a.m. on five nights of sampling (Figure 3E and 3F). Despite these attempts, it was not possible to capture the moth species during the observations.
Pollinators recorded on Discocactus ferricola flowers. A. Beetles inside flowers after anthesis. B. Beetles piercing the flower buds. The black arrow points to the beetles, and the red arrow points to the floral bud starting to emerge from the cephalium. C. Beetles of the Nitidulidae family inside the open flowers. D. Beetles of the Chrysomelidae family inside the open flowers. E-F. Moths visiting flowers.
Discussion
1. Species distribution modeling
In this study, we increased the number of known populations of D. ferricola from three to 11 populations. With the new occurrence sites, it was possible to construct a map of climatic suitability for the occurrence of D. ferricola based on ecological niche modeling. The area with the highest suitability identified by the model was concentrated mainly in the RPMU, which corroborates the high environmental specificity described for Discocactus species (Machado et al. 2005MACHADO, M.C., ZAPPI, D.C., TAYLOR, N.P. & BORBA EL. 2005. Taxonomy and conservation of the Discocactus Pfeiff. (Cactaceae) species occurring in the state of Bahia, Brazil. Bradleya 23:41-57.). Most of the area with high values of climatic suitability for D. ferricola in the RPMU is distributed continuously. Therefore, these areas of higher environmental suitability for D. ferricola may also represent possible dispersal routes among populations (Figure 2). We also observed small disconnected areas with climatic suitability for D. ferricola in the Serra do Amolar and on some nearby hills as well as in the Serra da Bodoquena. Currently, neither GBIF nor Species Link have records of D. ferricola at these localities, which may be the result of undersampling due to difficulty in accessing the areas of occurrence or even of a limited dispersion capacity of this species, preventing it from colonizing these regions even with an adequate climate for its occurrence. The potential distribution map highlighted areas with higher probability of occurrence of D. ferricola on the Residual Plateau of Maciço do Urucum, which concentrates the largest area with the highest climatic suitability among the analyzed rock formations, probably concentrating the largest number of populations. Due to the high environmental specificity of D. ferricola, it is advisable that searches for new populations be carried out in areas of shallow soils, sandy or exposed rock within the areas described with relatively high values of climatic suitability to optimize time and resources (Machado et al. 2005MACHADO, M.C., ZAPPI, D.C., TAYLOR, N.P. & BORBA EL. 2005. Taxonomy and conservation of the Discocactus Pfeiff. (Cactaceae) species occurring in the state of Bahia, Brazil. Bradleya 23:41-57.).
Among the 11 populations sampled, only two populations of D. ferricola were found inside a protected area (Piraputanga Municipal Park), although the area has no maintenance, inspection or access restrictions. The other nine populations were on farms accessible to cattle and subject to fire or close to mining. Therefore, all known D. ferricola populations are exposed to threats like habitat loss, wildfires, and extraction for consumption as food or by collectors due to their ornamental potential. The available information about the distribution of D. ferricola in the Red List of Threatened Species states an area of occurrence of no more than 20 km2 (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
https://dx.doi.org/10.2305/IUCN.UK.2013-...
). However, ironstone outcrops represent a total area of only 6.4 km2 distributed irregularly on the RPMU (Pott et al. 2000POTT, A., SILVA, J.S.V., SALIS, S.M., POTT, V. & SILVA, M.D. 2000. Vegetação e uso da terra. In Zoneamento ambiental da Borda Oeste do Pantanal: Maciço do Urucum e Adjacências (J.S.V. Silva, ed.). Embrapa, Brasília, p. 111-131.). Thus, it is possible that the area of occurrence of D. ferricola is much less than 20 km2 (Braun 2013BRAUN, P. 2013. The IUCN Red List of Threatened Species 2013: Discocactus ferricola. Available: https://dx.doi.org/10.2305/IUCN.UK.2013-1.RLTS.T151934A578020.en.
https://dx.doi.org/10.2305/IUCN.UK.2013-...
).
2. Pollinator dependence and floral visitors
The absence of fruits in the self-pollination treatments may have been the result of a self-incompatible reproductive system or of extreme inbreeding depression (Mandujano et al. 2010MANDUJANO, M.C., CARRILLO-ANGELES, I., MARTÍNEZ-PERALTA, C. & GOLUBOV, J. 2010. Reproductive biology of Cactaceae. In Desert Plants (K.G. Ramawat, ed.) Springer, Berlin/ Heidelberg, p.197-230.). Despite of the cause, our results indicated that D. ferricola is obligatory xenogamic, and depends on the action of pollinators for effective pollination to occur. Reproductive mechanisms that act to prevent inbreeding and the consequent loss of genetic diversity are often found in species of the family Cactaceae (Mandujano et al. 2010MANDUJANO, M.C., CARRILLO-ANGELES, I., MARTÍNEZ-PERALTA, C. & GOLUBOV, J. 2010. Reproductive biology of Cactaceae. In Desert Plants (K.G. Ramawat, ed.) Springer, Berlin/ Heidelberg, p.197-230.). Xenogamy has been described for several species of cacti, including species that occur in rocky outcrops such as Cipocereus minensis (Werderm.) Ritter, Uebelmannia buiningii Donald, Pilosocereus catingicola (Gürke) Byles & Rowley, P. chrysostele (Vaupel) Byles & G.D.Rowley, and P. pachycladus F.Ritter (Martins et al. 2016MARTINS, C., OLIVEIRA, R., MENDONÇA FILHO, C.V., LOPES, L.T., SILVEIRA, R.A., DE SILVA, J.A.P., AGUIAR L.M.S. & ANTONINI, Y. 2016. Reproductive biology of Cipocereus minensis (Cactaceae)-A columnar cactus endemic to rupestrian fields of a Neotropical savannah. Flora 218:62-67., Teixeira et al. 2018TEIXEIRA, V. D., VEROLA, C. F., DA COSTA, I. R., ZAPPI, D. C., DA COSTA, G. M., SILVA, S. R., COSTA M.A.P.C. & AONA, L.Y.S. 2018. Investigating the floral and reproductive biology of the endangered microendemic cactus Uebelmannia buiningii Donald (Minas Gerais, Brazil). Folia Geobot. 53(2):227-239., Rocha et al. 2020ROCHA, E.A., DOMINGOS-MELO, A., ZAPPI, D.C., & MACHADO, I.C. 2020. Reproductive biology of columnar cacti: are bats the only protagonists in the pollination of Pilosocereus, a typical chiropterophilous genus?. Folia Geobot. 54: 239-256.).
We found a lower number of seeds per fruit in the natural pollination treatment than in the manual pollination treatment, which suggests that the pollination function in D. ferricola may be inefficient due to a limitation in pollen deposition (Burd 1994BURD, M. 1994. Bateman’s Principle and plant reproduction: The role of pollen limitation in fruit and seed set. Bot. Rev. 60(1):83-139., Larson & Barret 2000LARSON, B.M.H. & BARRET, S.C.H. 2000. A comparative analysis of pollen limitation in flowering plants. Biol. J. Linn. Soc. 69(4):503-520.). This limitation could be caused by pollen of poor quality (flowers usually receive self-pollen, in addition to crossed pollen) or by the amount of pollen available (frequency of visits) (Aizen & Harder 2007AIZEN, M.A. & HARDER, L.D. 2007. Expanding the limits of the pollen‐limitation concept: effects of pollen quantity and quality. Ecology 88(2):271-281.). Pollen limitation is more frequent in self-incompatible species; in such cases, it is possible that the stochastic behavior of pollinators and local ecological conditions limit the activity of pollinators and are associated with reduced fertility (Burd 1994BURD, M. 1994. Bateman’s Principle and plant reproduction: The role of pollen limitation in fruit and seed set. Bot. Rev. 60(1):83-139., Larson & Barret 2000LARSON, B.M.H. & BARRET, S.C.H. 2000. A comparative analysis of pollen limitation in flowering plants. Biol. J. Linn. Soc. 69(4):503-520.). This may be the case of D. ferricola since we recorded only four moth visits, with flowers receiving no more than one visit, and because we found the species to be dependent on crossed pollen. Self-incompatibility and pollen limitation have also been described for Discocactus pseudoinsignis N.P.Taylor & Zappi and Discocactus placentiformis K.Schum., species that occur in Minas Gerais state, Brazil (Silveira 2015SILVEIRA R.A. 2015. Ecologia de Discocactus pseudoinsignis e Discocactus placentiformis simpátricos e endêmicos da Serra do Espinhaço, MG, Brasil. MSc Thesis, Universidade Federal de Ouro Preto, Ouro Preto. UFOP. http:// www.repositorio.ufop.br (last access 06/09/2020).
http:// www.repositorio.ufop.br...
).
Flowers of D. ferricola were visited by two species of beetles, one from the Nitidulidae family and another from the Chrysomelidae family, and by moths from the Sphingidae family. The presence of beetles on flowers is often considered negative, as they usually act as pollen/nectar harvesters and as consumers of flowers (Pimienta-Barrios & del Castillo 2002PIMIENTA-BARRIOS, E., & DEL CASTILLO, R.F. 2002. Reproductive Biology. In Cacti: Biology and Uses (P.S. Nobel, ed.). University of California, London, p.75- 90., Martínez-Peralta & Mandujano 2011MARTÍNEZ-PERALTA, C. & MANDUJANO, M.C. 2011. Reproductive ecology of the endangered living rock cactus, Ariocarpus fissuratus (Cactaceae). J. Torrey Bot. Soc. 138(2):145-155.). Studies on other cactus species from outcrops, such as Cipocereus laniflorus N.P.Taylor & Zappi, Pilosocereus catingicola subsp. salvadorensis (Werderm.) Zappi, and Micranthocereus purpureus (Gürke) F.Ritter, have also found small beetles piercing flower buds serving as pollen robbers and consuming floral parts mainly during anthesis and postanthesis stages, as found for D. ferricola in this study (Locatelli et al. 1997LOCATELLI, E., MACHADO, I.C. & MEDEIROS, P. 1997. Floral biology and bat pollination in Pilosocereus catingicola (Cactaceae) in northeastern Brazil. Bradleya 15:28-34., Pimienta-Barrios & Castillo 2002PIMIENTA-BARRIOS, E., & DEL CASTILLO, R.F. 2002. Reproductive Biology. In Cacti: Biology and Uses (P.S. Nobel, ed.). University of California, London, p.75- 90., Aona et al. 2006AONA, L.Y.S., MACHADO, M., PANSARIN, E.R., DE CASTRO, C.C., ZAPPI, D. & MARIA DO CARMO, E. 2006. Pollination biology of three Brazilian species of Micranthocereus Backeb. (Cereeae, Cactoideae) endemic to the “campos rupestres”. Bradleya 2006(24): 39-52., Rego et al. 2012REGO, J.O., FRANCESCHINELLI, E.V. & ZAPPI, D.C. 2012. Reproductive biology of a highly endemic species: Cipocereus laniflorus N.P. Taylor & Zappi (Cactaceae). Acta Bot. Bras. 26(1):243-250.).
In this study, moths were the only registered nighttime visitors and they did it in a low frequency (four visits recorded from camera traps). Although we could confirm the introduction of month proboscis in the flowers, we could not affirm from photos if they touched the stigma. However, the moth likely touches the stigma due to its location within the tubular corolla and the sphingophilous syndrome (Pimienta-Barrios & del Castillo 2002PIMIENTA-BARRIOS, E., & DEL CASTILLO, R.F. 2002. Reproductive Biology. In Cacti: Biology and Uses (P.S. Nobel, ed.). University of California, London, p.75- 90., Machado et al. 2005MACHADO, M.C., ZAPPI, D.C., TAYLOR, N.P. & BORBA EL. 2005. Taxonomy and conservation of the Discocactus Pfeiff. (Cactaceae) species occurring in the state of Bahia, Brazil. Bradleya 23:41-57.). In addition, the time of anthesis in D. ferricola restricts visits from nocturnal pollinators, as the flowers are still closed during early evening. Some cacti that have nocturnal anthesis extend the anthesis period until the morning of the following day (Fleming et al. 2001FLEMING, T. H., SAHLEY, C. T., HOLLAND, J. N., NASON, J. D. & HAMRICK, J. L. 2001. Sonoran Desert columnar cacti and the evolution of generalized pollination systems. Ecol. Monogr. 71(4):511-530.), as observed by Silveira (2015)SILVEIRA R.A. 2015. Ecologia de Discocactus pseudoinsignis e Discocactus placentiformis simpátricos e endêmicos da Serra do Espinhaço, MG, Brasil. MSc Thesis, Universidade Federal de Ouro Preto, Ouro Preto. UFOP. http:// www.repositorio.ufop.br (last access 06/09/2020).
http:// www.repositorio.ufop.br...
in D. pseudoinsignis and D. placentiformis, which keep flowers open until 11 a.m. of the next day, allowing visits from diurnal pollinators such as bees. Extending the anthesis period to diurnal hours increases the diversity of pollinators and may be related to greater reproductive success (Fleming et al. 2001FLEMING, T. H., SAHLEY, C. T., HOLLAND, J. N., NASON, J. D. & HAMRICK, J. L. 2001. Sonoran Desert columnar cacti and the evolution of generalized pollination systems. Ecol. Monogr. 71(4):511-530.).
Our study highlighted the benefits and practicalities of the use of ecological niche modeling and data on reproductive biology to guide new sampling efforts, identify threats, and to assist conservation and management initiatives of endangered species. Moreover, this information allow the construction of more assertive hypotheses about the evolution and dispersion of species. The potential distribution map showed that the RPMU represents the largest and most important area of distribution of D. ferricola, concentrating the largest number of populations. We also found small disconnected areas with climatic suitability for D. ferricola in the Serra do Amolar and the Serra da Bodoquena, which represents potential areas for future sampling.
Strengthening public policies for in situ and ex situ conservation of threatened species of cactus should be in the spotlight of conservation plans. For D. ferricola, in situ conservation actions should prioritize the maintenance of interactions with pollinators by preserving flora and fauna of rocky outcrops and adjacent forests. For that, there is the need for revitalization and implementation of reserves, parks, and ecological corridors in areas of greater environmental suitability. As ex situ actions, we recommend the expansion of inspection activities by environmental authorities concerning the illegal trade of threatened and endemic species. Our approach and results may assist in the evaluation and implementation of more efficient conservation actions for rare and endangered species, especially for D. ferricola.
Acknowledgments
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. We appreciate the financial support given to LVS (FUNDECT 59/300.508/2016 and Capes 88887.197188/2018-00). We also appreciate the financial support of the Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul (FUNDECT/CNPq no. 05/2011-PPP [23/200.659/2012] and FUNDECT/CAPES no. 44/2014-PAPOS-MS [23/200.039/2014 I and II]).
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Publication Dates
-
Publication in this collection
20 Dec 2021 -
Date of issue
2022
History
-
Received
13 Oct 2020 -
Accepted
11 Nov 2021