Abstract
Parodia carambeiensis is a rupicolous, small-sized species, with globose cladode and showy flowers, and is the only endemic Cactaceae species in Paraná State (Brazil). Changes in natural landscapes and fragmentation isolate populations, increasing their vulnerability to local extinctions. Our aim was to verify the spatial distribution of P. carambeiensis, reviewing its conservation status and main threats in the distribution area. Expeditions were carried out in the Campos Gerais region to record the abundance, density and spatial distribution of P. carambeiensis populations. Local landscape and climatic variables as well as the joint effect of these with geographical distance, were analyzed. Our findings highlighted that population density differs among the studied sites and was driven by distinct levels of anthropic threats such as livestock, tourism, wildfires and their proximity to highways, along with the climatic variables evaluated (temperature range and precipitation). The models jointly explained 56% of the variation in the population density, which was mostly influence by climatic factors. Parodia carambeiensis is currently classified as (LC) least concern, however, our results provide strong evidence in favor of updating its status to (EN) endangered due to the elevated extinction risk of natural populations.
Key words
anthropic actions; cactus; endemism; vulnerability
Resumo
Parodia carambeiensis é uma espécie rupícola de pequeno porte, com cladódio globoso e flores atrativas, sendo a única Cactaceae endêmica do estado do Paraná. As alterações das paisagens naturais e a fragmentação tem levado ao isolamento das populações deixando-as mais vulneráveis a extinções locais. Nosso objetivo foi verificar a distribuição espacial desta espécie, revisar seu status de conservação e principais ameaças ao longo da área de distribuição. Foram realizadas expedições na região dos Campos Gerais, relatando a abundância, densidade e distribuição espacial das populações. Foram conduzidas as análises das variáveis locais do ambiente e climáticas, bem como o efeito conjunto destas variáveis e a distância geográfica. Os resultados indicam uma variação da densidade populacional entre as localidades, e pode ser resultante das ações antrópicas locais como pecuária, turismo, queimadas e a proximidade com rodovia, além do clima considerando-se a amplitude térmica e precipitação. Os modelos avaliados em conjunto explicaram 56% de variação na densidade populacional, sendo os fatores climáticos os principais determinantes da distribuição desta espécie. Atualmente a espécie está classificada como pouco preocupante, entretanto sugere-se a mudança da categoria do status para em perigo, baseado na revisão dos dados atuais e alto risco de extinção na natureza.
Palavras-chave
ações antrópicas; cactus; endemismo; vulnerabilidade
Introduction
Cactaceae is represented by 129 genera and 1.450 species with neotropical distribution. According to current systematics, it is composed of four subfamilies: Pereskioideae, Maihuenioideae, Opuntioideae and Cactoideae (Hunt et al. 2006Hunt D, Taylor NP & Charles C (2006) The new cactus lexicon. DH Books. Milborne Port. 900p.; Zappi & Taylor 2020Zappi D & Taylor N (2020) Cactaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB70>. Access on 29 September 2020.
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). In Brazil, 81 genera and 484 species of Cactaceae have been recorded so far, of which 208 species are endemic (Zappi & Taylor 2020Zappi D & Taylor N (2020) Cactaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB70>. Access on 29 September 2020.
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).
Species of Cactaceae are mostly distributed in the American continent, except for Rhipsalis baccifera (Muell.) Stearn which occurs in Africa, being known by the success to colonize hostile environments that are generally not suitable for other plants, for example, those with substrates scarce in nutrients and water (Silva et al. 2011Silva SR, Zappi D, Taylor N & Machado M (2011) Plano de ação nacional para conservação de Cactáceas. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília. 58p.; Cavalcante et al. 2013Cavalcante A, Teles M & Machado M (2013) Cactos do semiárido do Brasil: guia ilustrado. INSA, Campina Grande. 53p.). They play important roles in ecosystems with low production and may contribute significantly to local food webs. Such plants provide succulent fruits, nectar and pollen, which are vital resources in xeric environments, supplying water and nutrients to a wide variety of animals (Cavalcante et al. 2013Cavalcante A, Teles M & Machado M (2013) Cactos do semiárido do Brasil: guia ilustrado. INSA, Campina Grande. 53p.).
The genus Parodia Speg. is distributed along Argentina, Paraguay, Uruguay, Bolivia and Brazil, being comprised by of 48 species, 18 of which are restricted to the south of Brazil, mainly in the States of Santa Catarina and Paraná with the higher levels of species richness observed in Rio Grande do Sul, in the Pampa and Atlantic Rainforest biomes (Carneiro et al. 2016; Zappi & Taylor 2020Zappi D & Taylor N (2020) Cactaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB70>. Access on 29 September 2020.
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). Parodia carambeiensis (Buining & Brederoo) Hofacker, is commonly known as “cactus-ball” globose stem, flowers with yellow tepals and pink stigma (Fig.1 a-b). Soller et al. (2014)Soller A, Soffiatti P, Calvente A & Goldenberg R (2014) Cactaceae no estado do Paraná, Brasil. Rodriguésia 65: 201-219. conducted a taxonomic study of Cactcaeae in the state of Paraná and found the occurrence of 12 genera and 26 native species, most epiphytes, inhabiting Atlantic Rainforest and Araucaria Forest, being P. carambeiensis the only endemic species of Cactaceae in the state of Paraná.
Campos Gerais region is located in the second plateau of Paraná, where the vegetation is part of the Atlantic Rainforest domain, but comprises a mosaic of forest fragments, grasslands and savanna remnants, combining the ecotones in a very particular way (Moro & Carmo 2014Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.). Despite the unique vegetational mosaic, these ecosystems have been severely threatened by forestation with exotic species, conversion of natural fields into monoculture, livestock, wildfires, excessive and illegal collections, as well as the impacts of tourism (Ziller & Galvão 2002Ziller SR, Galvão FA (2002) A degradação da estepe gramíneo-lenhosa no Paraná por contaminação biológica de Pinus elliottii e P. taeda. Floresta 32: 41-47.; Linsingen et al. 2006Linsingen LV, Sonehara JS, Uhlmann A & Cervi A (2006) Composição florística do Parque Estadual do Cerrado de Jaguariaíva, Paraná, Brasil. Acta Biológica Paranaense 35: 197-232.).
On a broad scale, the distribution of P. carambeiensis is limited by patches of rocky outcrops, featured by shallow soils with water deficiency, for which this species’ morpho-anatomy is well adapted to (Moro & Carmo 2014Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.). On a local scale, like most Cactaceae, P. carambeiensis presents clumped distribution as consequence of concentrated resource allocation within heterogeneous environments (Godínez et al. 2003Godínez AH, Valverde T & Ortega BP (2003) Demographic Trends in the Cactaceae. The Botanical Review 69: 173-203. ) (Fig. 1c). This species is also associated with species of the genus Calea L. (Asteraceae), Andropogon L. (Poaceae), Dyckia Schult. & Schult.f (Bromeliaceae) and mosses, which inhabit rocky outcrops in the Campos Gerais. Such plants are usually called “nurse plants” since they support the development of cacti and other plants in the outcrops by providing a more suitable microenvironment, with improved water supply and limited solar exposition (Flores & Jurado 2003Flores J & Jurado E (2003) Are nurse-protégé interactions more common among plants from arid environments? Journal of Vegetation. Science 14: 911-916.; Oliveira 2009).
a-f. Characteristics of Parodia carambeiensis, Campos Gerais, PR (Brazil). – a. flowers; b. lanugo as an indication of maturity; c. a local subpopulation; d. influence of Pinus spp; e. occurrence of recent wildfire in one study site; f. agriculture.
Cactaceae is the fifth most threatened plant family in Brazil, mainly due to its high endemism, endemic distribution and ornamental value, leading to a large number of vulnerable or threatened species (Hinostrosa & Hernandez 2000Hinostrosa CG & Hernandez HM (2000) Diversity, geographical distribution and conservation of Cactceae in the Mier y Noriega region, Mexico. Biodiversity and Conservation 9: 403-418.; Ortega & Godínez 2006; Silva et al. 2011Silva SR, Zappi D, Taylor N & Machado M (2011) Plano de ação nacional para conservação de Cactáceas. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília. 58p.; Goettsch et al. 2015Goettsch B, Hilton-Taylor C, Cruz-Piñón G, Duffy JP, Frances A, Hernández HM, Inger R, Pollock C,Schipper J, Superina M, Taylor NP, Tognelli M, Abba AM, Arias S, Arreola-Nava HJ, Baker MA, Bárcenas RT, Barrios D, Braun P, Butterworth CA, Búrquez A, Caceres F, Chazaro-Basañez M, Corral- Díaz R, Perea MV, Demaio PH, Duarte de Barros WA, Durán R, Yancas LF, Felger RS, Fitz-Maurice B, Fitz-Maurice WA, Gann G, Gómez-Hinostrosa C, Gonzales-Torres LR, Griffith MP, Guerrero PC, Hammel B, Heil KD, Hernández-Oria JG, Hoffmann M, Ishihara MI, Kiesling R, Larocca J, León de la Luz JL, Loaiza CR, Lowry M, Machado MC, Majure LC, Ávalos JGM, Martorell C, Maschinski J, Méndez E, Mittermeier RA, Nassar JM, Negrón- Ortiz V, Oakley LJ, Ortega-Baes P, Ferreira ABP, Pinkava DJ, Porter JM, Puente-Martinez R, Gamarra JR, Pérez PS, Martínez ES, Smith M, J Manuel Sotomayor M Del C, Stuart SM, Muñoz JLT, Terrazas T, Terry M, Trevisson M, Valverde T, Devender TRV, Véliz-Érez ME, Walter HE, Watt SA, Zappi D, Zavala-Hurtado JA & Gaston KJ (2015) High proportion of cactus species threatened with extinction. Nature Plants 15142: 1-7.). Currently, Parodia carambeiensis is categorized as Least Concern (LC) according to IUCN criteria (Larocca & Machado 2017Larocca J & Machado M (2017) Parodia carambeiensis (amended version of 2013 assessment). The IUCN Red List of Threatened Species 2017. Available at <https://dx.doi.org/10.2305/IUCN.UK.20173.RLTS.T152583A121600482.en>. Access on 23 April 2020.
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), although a recent review suggested a new classification as Vulnerable (VU) (Anceschi & Magli 2018Anceschi G & Magli A (2018) A synopsis of the genus Parodia Spegazzini s.I (Cactaceae). Bradleya 36: 70-161.).
The current IUCN classification considers the presence of P. carambeiensis subpopulations in protected areas, which in turn decreases extinction risks. However, small and isolated populations are more vulnerable to local extinctions over time due to lower genetic variability, with barriers to dispersion and pollination causing low reproductive success (Ricklefs 2010Ricklefs RE (2010) A economia da natureza. Ed. Guanabara, Rio de Janeiro. 572p.). Therefore, preserving sustainable populations in diverse habitat patches can increase the capacity for recolonization and rescue populations that occasionally become more vulnerable (Begon et al. 2007Begon M, Townsend CR & Harper JL (2007) Ecologia de indivíduos a ecossistemas. Artmed, Porto Alegre. 740p.).
In order to review the current conservation status and threats of P. carambeiensis, we aimed to report the main anthropogenic threats influencing the distribution and density of this species throughout the Campos Gerais area, how well conservation units protect it, as well as the influence of climatic factors and geographic distance on its distribution and density.
Material and Methods
Study area
The research was conducted within the Campos Gerais domain, encompassing 22 municipalities spread over the second plateau of Paraná, with total extension of 11,741.41 km2, lying between 23°45’S and 26°15’S latitude and 49°15’W and 50°45’W longitude (Melo et al. 2014Melo MS, Moro RS & Guimarães GB (2014) Patrimônio natural dos Campos Gerais. UEPG, Ponta Grossa. 233p.) (Fig. 2).
Distribution and occurrence maps of Parodia carambeiensis based on the sampling sites and herbaria data from the Paraná State. The municipalities of the studied sites are also indicated on the map.
To assess populational distribution and density, the surveys were performed on 12 plots distributed in five municipalities in the area names as Campos Gerais, a geographic region restricted between Escarpa Devoniana and Escarpa da Esperança (Maack 2012Maack R (2012) Geografia física do estado do Paraná. 4º ed. UEPG, Ponta Grossa. 526 p. ). This region is characterized by extent areas of grassland, comprised by Atlantic Rainforest and Cerrado biomes, with open fields and rocky outcrops associated with forest remmants and savannah formations (Moro & Carmo 2014Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.; Sema 2018Sema (2018) Conhecendo o bioma Mata Atlântica. Revista Atlântica 1: 1-20.). The soil is composed by sedimentary rocks, arenites and shales, classified as shallow and poor (Sá 2014Sá MFM (2014) Solos. In: Melo MS, Moro RS & Guimarães GB Patrimônio Natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 73-83.). Ponta Grossa, Lapa, Palmeira, Carambeí and Tibagi are the municipalities covered in the study, which also included private and public conservation units such as “Parque Estadual do Canyon Guartelá” and “RPPN Sonho Meu” (Tibagi), Parque Estadual de Vila Velha (Ponta Grossa), and Parque Estadual do Monge (Lapa), as well as plots located on private lands (Tab. 1). Most localities are located within the environmental protection area of Escarpa Devoniana and some are inside Parque Nacional dos Campos Gerais.
Distribution and occurrence sites of Parodia carambeiensis based on herbarium data and field expeditions in the Campos Gerais region, state of Paraná, 2017.
In order to redraw the new conservation status, a distribution map was developed based on data records from herbaria collections and field samples, totaling 26 occurrence sites in Paraná state (Tab.1).
Samplings
Field expeditions were performed in the Campos Gerais region between March and August 2017. The studied sites were defined based on prior cacti occurrence reports, thus several surveys were conducted in habitats that are suitable for cacti development, e.g., rocky outcrop, between rock crevices, (rupicolous) and soil patches. During the expeditions, a specimen was collected and deposited into the Herbarium of the State University of Ponta Grossa (HUPG) as voucher material.
The field surveys were performed at 11 sites where the cactus was recorded in the five municipalities previously cited. In each area, six (6) 10 m × 10 m parcels were defined, with a total scanning area of 600 m2 per site. At each site, the parcels were distributed according to an active search of the populations, with mature forms counted inside a given parcel, based on Ribeiro (2011)Ribeiro EMS (2011) Influências de perturbações antrópicas sobre população de Cactaceae em áreas de Caatinga. Dissertação de Mestrado. Universidade Federal de Pernambuco, Recife. 67p..
Mature individuals were determined based on size, with height higher than 50 mm, presence of white fluff on the top (indicating the beginning of the reproductive phase) (Fig. 1c), remnants of floral structures and presence of fruits (Soller et al. 2014Soller A, Soffiatti P, Calvente A & Goldenberg R (2014) Cactaceae no estado do Paraná, Brasil. Rodriguésia 65: 201-219.).
In each parcel, a set of local environmental factors that could influence the distribution and density of cacti were recorded, listed as follows: the presence of native vegetation, exotic plants, farming, deforestation, livestock, litter from ecotourism, recent wild fires, presence of roads nearby, presence of rivers and lakes nearby. The choice of the set of local variables was based on previous literature and studies referring to anthropic actions on cacti species (Silva et al. 2011Silva SR, Zappi D, Taylor N & Machado M (2011) Plano de ação nacional para conservação de Cactáceas. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília. 58p.), and about the local threatens to the native vegetation (Moro & Carmo 2014Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.).
Climatic variables
Climate data from each site was obtained from the Worldclim website (<http://www.worldclim.org/>), with a resolution of 30 seconds (1km2) (Fick & Hijmans 2017Fick SE & Hijmans RJ (2017) Worldclim 2: New 1- km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302-4315.). The set of climatic variables included variations in temperature and precipitation data for each site (annual monthly average temperature, maximum and minimum temperature, temperature range, total annual precipitation, average monthly precipitation, driest monthly precipitation, precipitation in wettest month, among others with a total of 19 bioclimatic variables). These variables were evaluated for collinearity among themselves (correlation between variables). Therefore, the VIF values (variance inflation factor) for each variable were estimated, only retaining variables with values of < 2 VIF for analysis, i.e. those with little or no correlation to each other (Zuur et al. 2010Zuur AF, Leno EN & Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3-14.), such as annual mean temperature (BIO1), mean diurnal range (mean of monthly (max temp – min temp)) (BIO2), temperature annual range (max temperature of warmest month – min temperature of coldest month) (BIO7) and annual precipitation (BIO12).
Data analysis
In order to compare the average abundance of individuals in the study areas, we conducted an analysis of variance (ANOVA one way), followed by Tukey test a posteriori for pairwise differentiation. To evaluate the effect of local environmental variables (presence of rivers, conservation units, presence of invasive plants (e.g. Pinus spp.) (Fig. 1d), highways, ecotourism, livestock, agriculture and wildfires (Fig.1 e-f) an ANOVA was performed for each of the factors assessed. For example, the average number of individuals in sites where invasive plants were present and sites without this influence were recorded.
The effects of local and climatic variables on P. carambeiensis were evaluated by developing generalized linear models (GLMs), making it possible to assess which set of variables drive distribution and density of the cacti. In this sense, explanatory models were developed with different sets of variables, using those with the lowest akaike (AIC) values and highest degree of explanation (delta weight) (Burnham & Anderson 1998).
In order to check the relative importance of each set of variables on different spatial scales, we carried out a partial variation partitioning analysis (RDA redundancy analysis). This verified the partial effect of geographical distance (considering latitude and longitude as variables, macro-scale sense), climate factors (meso-scale), and local elements of the landscape (presence of invasive plants, agriculture, ecotourism (micro-scale) on the distribution and population densities of Parodia carambeiensis. Before the analysis of variance (ANOVA), the normality of variables was checked using the Shapiro-Wilk test. Besides the ANOVA, the GLM and RDA analyzes were performed in the R Software (2014).
Distribution pattern
The spatial distribution pattern of Parodia carambeiensis (as aggregated or clumped, random and uniform) was calculated from the coefficient of dispersion (CD) and Green Index (GI), which evaluates the ratio between the variance and mean abundance values. A CD equal to one (= 1) denotes a population with random distribution, CD <1 indicates population with uniform distribution, while CD >1 indicates an aggregate (or clumped) distribution (Brower et al. 1998). Considering the Green Index (GI), positive values indicate aggregate distribution, negative ones indicate random distribution and those equal to zero indicate uniform distribution (Ludwig & Reynolds 1988).
Conservation status
The spatial distribution map was created using data from the field surveys and assembled from the following herbaria collections in the Paraná State: UTFPR- HCF (Herbarium of Universidade Tecnológica Federal do Paraná Campus Campo Mourão), MBM (Botanical Museum Municipal de Curitiba), UFPR- UPCB (Herbarium of Universidade Federal do Paraná), HUPG (Herbarium of Universidade Estadual de Ponta Grossa), online version available Taxonline (<https://taxonline.bio.br/specieslink.php>).
The risks of extinction were estimated considering the criteria established by the International Union for Conservation of Nature-IUCN on a regional and national context (IUCN 2019IUCN (2019) Guidelines for using the IUCN Red List Categories and Criteria: version 14. Prepared by the Standards and Petitions Committee. IUCN. 113p.). The following factors were considered: population reductions, extent of occurrence, degree of isolation, area of occupancy, extent of anthropic impact on the number of populations, as well as the population density and spatial distribution map.
Thus, to reassess the conservation status of P. carambeiensis, we estimated the Extent of Occurrence (OE) and its Occurrence Area (OA) based on the recent dataset assembled by field surveys and available herbaria data. For OE, the entire (shortest) perimeter of the distribution area, including all occurrence points of P. carambeiensis records, was estimated. The occupancy area (OA) was estimated using Quantum GIS Program 2.0.1, by putting a mesh grid (4km2 area) on top of a species distribution map. This area corresponds to the sum of the checkered areas where the species can be found.
Results
Population density
The average abundance of P. carambeiensis differed among sites, with the highest densities found in Tacinha - Ponta Grossa (45.3 cacti/m2), and RPPN Sonho Meu – Tibagi (38.0 cacti/m2), near the Parque Estadual do Cânion Guartelá, and Cachoeira da Mariquinha - Ponta Grossa (26.5 cacti/m2). At other sites, the average density ranged from 1.4 to 10.0 cacti/m2, with the smallest average found in the Parque Estadual do Monge (Tab. 2).
Abundance of Parodia carambeiensis for each parcel (100m2), with mean ± standard error (SE) and dispersion index per site.
Although P. carambeiensis was found within the boundaries of some conservation units e.g., RPPN Sonho Meu, Parque Estadual de Vila Velha, and Parque Estadual do Monge, the highest population densities were still found on private properties in the areas surrounding the conservation units. The sites located in private domains have been experiencing intense anthropogenic pressure, enhancing the risks of local extinction, with isolation and fragmentation of habitats also increasing these chances.
Most populations of P. carambeiensis presented clumped distribution patterns since CD values ranged from 2.87 to 36.70 (Tab. 2). Only two sites fit in the uniform distribution pattern: Fazenda Modelo (CD=0.89), and Pedra Solitária (CD=0.98). However, considering the Green Index (GI), which complements the dispersion coefficient (CD), all the populations evaluated fit in a clumped pattern, except those from Fazenda Modelo which remained uniform.
Local and climatic variables
Populations of P. carambeiensis have been affected by changes in the natural landscape driven by anthropogenic actions (Fig.1 d-f). We found that the presence of roads nearby had a strongly negative effect on population densities, in addition, tourism and exotic or invasive species also tended to contribute negatively to cacti density (Tab. 3). On the other hand, presence of livestock, light wildfires, and lakes and rivers nearby seemed to contribute positively to population density (Tab.3).
Mean abundance ± standard error of P. carambeiensis according to the presence or absence of a given effect. Means were compared by a variance analysis (ANOVA).
Considering the influence of the climatic variables on the distribution and density of P. carambeiensis, we observed that annual average temperature (BIO1), annual thermal amplitude (BIO2) and annual average precipitation (BIO12) were the main drivers for population. Additionally, according to the generalized linear models (GLMs), the populational density was best explained by the model that accounts for the combined effect of local and climatic variables, including recent wildfires (Z = 49.97; p <0.001) (Fig. 3a), the occurrence of rivers/lakes near the sampling sites (Z =-25.87; p < 0.001) (Fig. 3b), annual thermal amplitude (R2 =0.29; Z = 55.46; p <0.001) (Fig. 3c) and average precipitation (R2 =0.03; Z = 25.03; p <0.001)(Fig. 3d).
Variation in the observed abundance of Parodia carambeiensis according to climatic and local influences as a result of the general linear model test (GLM).
Combined effects on macro, meso and micro scales
The variation partitioning analysis (RDA) highlighted that 56% (R2 = 0.56) of the variation in P. carambeiensis density could be explained by the set of variables evaluated in the study. The total explanation percentage considers the importance of structuring components on a local scale (e.g., presence of roads, lakes and rivers, livestock and wildfires), which accounted for 14% of the explanation (R2 = 0.14), while macro-scale components (geographical distance among the sites) accounted for 18% of the explanation (R2 = 0.18). Finally, the meso-scale components (represented by the climatic variables) accounted for 24% (R2 = 0.24) of explanation.
Conservation status
According to IUCN criteria and the dataset about geographical distribution and occurrence of P. carambeiensis, this species fits into category B, which corresponds to taxa with restricted geographical distribution in fragmentated habitats, and declining or fluctuating populations. The species is distributed over an extension area of 23,276 km2, however, only occupies 168 km2. Notwithstanding, the results indicate that P. carambeiensis must be considered an Endangered species (EN), since it presents restricted distribution and is threatened by anthropic influences (IUCN criteria: EN: B2ab, iii, iv, v).
Discussion
The results demonstrate that populational density and spatial distribution of P. carambeiensis are ruled by a set of variables including local anthropic influences, climate variables and geographic distance.
Anthropic threats such as deforestation, fragmentation and conversion of natural lands for agriculture and livestock use are the leading causes of species extinction (Pimm et al. 1995Pimm SL, Russell GJ, Gittleman JL & Brooks TM (1995) The future of biodiversity. Science 269: 347-350.; Gurevitch et al. 2009Gurevitch J, Scheiner SM & Fox GA (2009) Ecologia Vegetal. Ed. Porto Alegre, Artmed. 592p.). Cultivation of exotic species such as Eucalyptus spp. and Pinus spp. affects at least 27 native plant species in the southern Brazil, including threatened species such as Parodia muricata (Otto ex Pfeiff.) Hofacker (Goettesch et al. 2015). Pine cultivation is one of the main crops in the Campos Gerais region, and, in addition to the conversion of natural areas, the seeds of this species are easily dispersed by the wind, making it a harmful invasive species in natural areas where it competes with native vegetation and increases extinction risks and native biodiversity loss (Neto & Rocha 2014Neto PHW & Rocha CH (2014) Caracterização da produção agropecuária e implicações ambientais nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. Ed. UEPG, Ponta Grossa. Pp. 182-190.; Rocha & Neto 2014Rocha CH & Neto PHW (2014) Origens dos sistemas de produção e fragmentação da paisagem nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio Natural dos Campos Gerais do Paraná. Ed. UEPG, Ponta Grossa. Pp. 171-180.).
Furthermore, areas of scenic natural beauty within the Campos Gerais region intrigue tourists and increase visitation in the region, which could have a negative effect on endangered species, especially P. carambeiensis, as highlighted. Whenever tourism and visitation are not regulated and sustainable, they can threaten natural ecosystems by decreasing populations, which is what was observed for this cactus. The main threats may be caused by direct impacts as trampling, crushing and uprooting, or indirect impacts such as environmental degradation, fires, the activities and behavior of native animals, pollinators, changes in soil biota including fungi and nutrients, and hydrology (Liddle 1997Liddle MJ (1997) Recreation ecology. Chapman and Hall, London. 664p.; Buckley 2004Buckley R (2004) Environmental impacts of tourism. CABI International, New York. 389p.; Pickering & Hill 2007Pickering CM & Hill W (2007) Impacts of recreation and tourism on plant biodiversity and vegetation in protected areas in Australia. Journal of Environmental Management 85:791-800.). The presence of highways near the areas also had a negative effect on these populations, since they facilitate human access and tourism in the sites, as well as act as barriers between habitat patches, hindering seed dispersion and pollination (Forman et al. 2003Forman RTT, Sperling D, Bissonette JA, Clevenger AP, Cutshall, CD, Dale VH, Fahrig L, France R, Goldman CR, Heanue K, Jones JA, Swanson FJ, Turrentine T & Winter TC (2003) Road ecology science and solutions. Island Press, Washington, DC. 481p. ).
Nevertheless, our data agrees with Ortega et al. (2010) & Méndez et al. (2004)Méndez M, Durán R Olmsted I & Oyoama K (2004) Population dynamics of Pterocereus gaumeri, a rare and endemic columnar cactus of Mexico. Biotropica 36: 492-504., who highlighted that some anthropic actions may also enhance the occurrence and densities of Cactaceae. For example, the presence of livestock in areas near the studied sites had a peculiar influence and positively affected P. carambeiensis population densities. Studies by Martorell & Peters (2009)Martorell C & Peters E (2009) Disturbance- response analysis: a Method for rapid assessment of the threat to species in disturbed áreas. Conservation Biology 23: 377- 387. on the genus Mammillaria Haw. (Cactaceae) indicated that most species of this genus present high densities in areas near pastures. These studies help understand P. carambeiensis better because the RPPN Sonho Meu (Tibagi) is associated with cattle breeding sites, which could be providing an extra source of nutrients for the cacti and favoring population increase.
Similarly, we also found out that past wildfires also positively affected P. carambeiensis density, which could be due to the elimination of competitors and exotic species such as Melinis minutiflora P. Beauv. (Poaceae) (Martins et al. 2011Martins CR, Hay JDV, Walter BMT, Proença CEB & Vivaldi LJ (2011) Impacto da invasão e do manejo do capim-gordura (Melinis minutiflora) sobre a riqueza e biomassa da flora nativa do Cerrado sentido restrito. Brazilian Journal of Botany 34: 73-90.), which is one of main threatens to the local vegetation (Moro & Carmo 2014Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.). However, studies by Silva et al. (2011) report that sites with high intensity and frequent fires are negatively correlated to native Cactaceae populations, as they impair reproduction and survival in the environment. Bowman et al. (2009)Bowman DMJS, Balch JK, Artaxo P, Bond WJ, Carlson JM, Cochrane MA, Antonio CMD, Defries RS, Doyle JC, Harrison SP, Johnston FH, Keeley JE, Krawchuk MA, Kull CA, Marston JB, Moritz MA, Prentice IC, Roos CI, Scott AC, Swetnam TW, Werf GR Van Der, Pyne SJ (2009) Fire in the Earth System. Science. 481-484. and Durigan & Ratter (2015)Durigan G & Ratter JA (2015) The need for a consistent fire policy for Cerrado conservation. Journal of Applied Ecology 53: 11-15. also highlight the unknown effect of fire on the ecosystem processes mainly when it is not managed. Hence, more studies about how population dynamics of P. carambeiensis and entire ecosystems are influenced by wildfire occurrences are needed.
The results of the General Linear Models (GLM) corroborated the importance of some local influences from analysis of variance (ANOVA) in addition to climatic variables (meso-scale elements). According to studies of plant communities, the outputs highlighted that the thermal amplitude and rainfall were important for modeling population density (Santos & Oliveira 2008). The seasonal variation in temperature was important in the models, with higher temperature variation throughout the year correlated to higher density of P. carambeiensis. Cactaceae are adapted to environments with wide thermal ranges (Steenbergh & Lowe 1977Steenbergh WE & Lowe CH (1977) Ecology of the saguaro: II, Reproduction, germination, establishment, growth, and survival of the young plant. Department of the Interior, National Park Service Scientific Monograph Series, Washington. 226p. ), with P. carambeiensis seeming to follow such same pattern, presenting higher densities in sites with wider temperature ranges throughout the year. Associated to this, rainfall had a weak positive influence on the populations, where sites with higher precipitation presented a slightly higher cactus density.
Data comprising meso and macro scale variables (climatic effect and geographic points) accounted for 24 and 18% of explanation about the variation in P. carambeiensis, density, respectively. This dataset is vital for modeling the distribution and occurrence of this species throughout the Campos Gerais region, since understanding the main drivers of spatial distribution allow the occurrence limits to be precisely defined. Such information is important to guide the action and conservation efforts in wide landscapes and to integrate occurrence patches.
Micro-scale or local elements explained 14% of P. carambeiensis density, being related to anthropic effects on the landscape. Notwithstanding, anthropic effects seem to have a relatively small effect on the cacti population and could be managed at local scales, resulting in the preservation of local populations with small densities. Considering our results, the main efforts must be focused on conserving isolated populations outside the conservation units and in the private areas, since they shelter most abundant populations and are more susceptible to anthropic threats. Meanwhile, it is important to develop strategies to enhance the connectivity between population patches, reducing the chances of local extinction and allowing dispersion and recolonization of empty areas, as well as for conservation measures such as species reintroduction and local management (Hanski & Gaggiotti 2004Hanski I & Gaggiotti OE (2004) Ecology, genetics, and evolution in metapopulations. Elsevier Academic Press. San Diego. 696 p.; Salazar & Moreira 2019Salazar CRL & Moreira NM (2019) Nuevo registro de Melocactus peruvianus (Cactaceae) y estado de conservación del género Melocactus en el Ecuador. Rodriguésia 70: 2-9.).
The clumped distribution of P. carambeiensis, typical of most Cactaceae, may be associated with the heterogeneous habitat found in Campos Gerais and also with the presence and type of soil in the rocky outcrop areas, these factors may be important for the occurrence of the species (Godínez et al. 2003Godínez AH, Valverde T & Ortega BP (2003) Demographic Trends in the Cactaceae. The Botanical Review 69: 173-203. ). This distribution pattern, along with the high degree of endemism, make P. carambeiensis more vulnerable (Ortega et al. 2010Ortega BP, Suring S, Sajama J, Sotola E, Alonso PM, Bravo S & Godínez AH (2010) Diversity and conservation in the Cactus family. In: Ramawat KG (ed.) Desert plants: biology and biotechnology. Springer, New York. Pp 157-173.; Menezes & Silva 2015).
According to the IUCN, P. carambeiensis is currently considered unconcerned (LC), which is used for taxon that present wide distribution or restricted distribution without significant threats. However, our outcomes highlighted that P. carambeiensis suffers from significant anthropogenic actions, with negative influences on their densities. Therefore, since most populations are distributed in sites without environmental protection and with high negative anthropic effects, suggesting that the species should be recategorized as endangered (EN). Goettsch et al. (2015) studied more than 1478 species of Cactaceae and reported a high concern about their current conservation status since it is among the most threatened plant families, being the habitat losses, invasive species and illegal collection the main causes of extinction.
In general, a major concern about the conservation status of Cactaceae is the combined effects of negative anthropic actions that lead to population isolation, increasing the vulnerability and extinction risks for this species (Hinostrosa & Hernández 2000; Contreras & Valverde 2002Contreras C & Valverde T (2002) Evaluation of the conservation status of a rare cactus (Mammillaria crucigera) through the analysis of its population dynamics. Elsevier Science 51: 89-102. ; Tapia et al. 2005Tapia RC, Mandujano MC, Valverde T, Mendoza A & Freaner FM (2005) How important is clonal recruitment for population maintenance in rare plant species? The case of the narrow endemic cactus, Stenocereus eruca, in Baja California, México. Elsevier Science 125: 123-132.). The new conservation status of P. carambeiensis arises from increased fragmentation in Campos Gerais, which in turn affects the populational conservation. Fragmentation and modification of a habitat can threaten local populations, drastically affecting the surviving, nutrients cycling, evapotranspiration and gene flow, with negative consequences to populations (Grilli et al. 2015Grilli J, Barabás G & Allesina S (2015) Metapopulation persistence in random fragmented landscapes. Plos Computational Biology 11: 1-13.; Martorell & Peters 2009Martorell C & Peters E (2009) Disturbance- response analysis: a Method for rapid assessment of the threat to species in disturbed áreas. Conservation Biology 23: 377- 387.).
Conclusions
Overall, our work provides an overview of the influences and threats that affect Parodia carambeiensis and suggests updating its conservation status to Endangered. Such update in conservation status reinforces the need to implement management measures that aim to protect this species and preserve Campos Gerais region, as this species is endemic and a symbol within this region.
Acknowledgements
We thank the Universidade Estadual de Ponta Grossa (UEPG) for their support and interest in this project. We thank Thais da Silva for collaboration with field surveys and Tainá Jardim Antunes (Universidade Federal do Sul da Bahia) for her valuable contributions in the preparation of the maps. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
References
- Anceschi G & Magli A (2018) A synopsis of the genus Parodia Spegazzini s.I (Cactaceae). Bradleya 36: 70-161.
- Begon M, Townsend CR & Harper JL (2007) Ecologia de indivíduos a ecossistemas. Artmed, Porto Alegre. 740p.
- Bowman DMJS, Balch JK, Artaxo P, Bond WJ, Carlson JM, Cochrane MA, Antonio CMD, Defries RS, Doyle JC, Harrison SP, Johnston FH, Keeley JE, Krawchuk MA, Kull CA, Marston JB, Moritz MA, Prentice IC, Roos CI, Scott AC, Swetnam TW, Werf GR Van Der, Pyne SJ (2009) Fire in the Earth System. Science. 481-484.
- Buckley R (2004) Environmental impacts of tourism. CABI International, New York. 389p.
- Burham KP & Anderson DR (1998) Model selection and inference: a practical information. Theoretic Approach, New York. 353p.
- Brower JE & Zar JH (1984) Field & laboratory methods for general ecology. McGraw-Hill, Boston. 226p.
- Cavalcante A, Teles M & Machado M (2013) Cactos do semiárido do Brasil: guia ilustrado. INSA, Campina Grande. 53p.
- Contreras C & Valverde T (2002) Evaluation of the conservation status of a rare cactus (Mammillaria crucigera) through the analysis of its population dynamics. Elsevier Science 51: 89-102.
- Durigan G & Ratter JA (2015) The need for a consistent fire policy for Cerrado conservation. Journal of Applied Ecology 53: 11-15.
- Fick SE & Hijmans RJ (2017) Worldclim 2: New 1- km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37: 4302-4315.
- Flores J & Jurado E (2003) Are nurse-protégé interactions more common among plants from arid environments? Journal of Vegetation. Science 14: 911-916.
- Forman RTT, Sperling D, Bissonette JA, Clevenger AP, Cutshall, CD, Dale VH, Fahrig L, France R, Goldman CR, Heanue K, Jones JA, Swanson FJ, Turrentine T & Winter TC (2003) Road ecology science and solutions. Island Press, Washington, DC. 481p.
- Godínez AH, Valverde T & Ortega BP (2003) Demographic Trends in the Cactaceae. The Botanical Review 69: 173-203.
- Goettsch B, Hilton-Taylor C, Cruz-Piñón G, Duffy JP, Frances A, Hernández HM, Inger R, Pollock C,Schipper J, Superina M, Taylor NP, Tognelli M, Abba AM, Arias S, Arreola-Nava HJ, Baker MA, Bárcenas RT, Barrios D, Braun P, Butterworth CA, Búrquez A, Caceres F, Chazaro-Basañez M, Corral- Díaz R, Perea MV, Demaio PH, Duarte de Barros WA, Durán R, Yancas LF, Felger RS, Fitz-Maurice B, Fitz-Maurice WA, Gann G, Gómez-Hinostrosa C, Gonzales-Torres LR, Griffith MP, Guerrero PC, Hammel B, Heil KD, Hernández-Oria JG, Hoffmann M, Ishihara MI, Kiesling R, Larocca J, León de la Luz JL, Loaiza CR, Lowry M, Machado MC, Majure LC, Ávalos JGM, Martorell C, Maschinski J, Méndez E, Mittermeier RA, Nassar JM, Negrón- Ortiz V, Oakley LJ, Ortega-Baes P, Ferreira ABP, Pinkava DJ, Porter JM, Puente-Martinez R, Gamarra JR, Pérez PS, Martínez ES, Smith M, J Manuel Sotomayor M Del C, Stuart SM, Muñoz JLT, Terrazas T, Terry M, Trevisson M, Valverde T, Devender TRV, Véliz-Érez ME, Walter HE, Watt SA, Zappi D, Zavala-Hurtado JA & Gaston KJ (2015) High proportion of cactus species threatened with extinction. Nature Plants 15142: 1-7.
- Grilli J, Barabás G & Allesina S (2015) Metapopulation persistence in random fragmented landscapes. Plos Computational Biology 11: 1-13.
- Gurevitch J, Scheiner SM & Fox GA (2009) Ecologia Vegetal. Ed. Porto Alegre, Artmed. 592p.
- Hanski I & Gaggiotti OE (2004) Ecology, genetics, and evolution in metapopulations. Elsevier Academic Press. San Diego. 696 p.
- Hinostrosa CG & Hernandez HM (2000) Diversity, geographical distribution and conservation of Cactceae in the Mier y Noriega region, Mexico. Biodiversity and Conservation 9: 403-418.
- Hunt D, Taylor NP & Charles C (2006) The new cactus lexicon. DH Books. Milborne Port. 900p.
- IUCN (2019) Guidelines for using the IUCN Red List Categories and Criteria: version 14. Prepared by the Standards and Petitions Committee. IUCN. 113p.
- Larocca J & Machado M (2017) Parodia carambeiensis (amended version of 2013 assessment). The IUCN Red List of Threatened Species 2017. Available at <https://dx.doi.org/10.2305/IUCN.UK.20173.RLTS.T152583A121600482.en>. Access on 23 April 2020.
» https://dx.doi.org/10.2305/IUCN.UK.20173.RLTS.T152583A121600482.en - Liddle MJ (1997) Recreation ecology. Chapman and Hall, London. 664p.
- Linsingen LV, Sonehara JS, Uhlmann A & Cervi A (2006) Composição florística do Parque Estadual do Cerrado de Jaguariaíva, Paraná, Brasil. Acta Biológica Paranaense 35: 197-232.
- Ludwid JA & Reynolds JF (1988) Statistical ecology. A primer on methods and computing. Wiley, Nova Iorque. 352p.
- Maack R (2012) Geografia física do estado do Paraná. 4º ed. UEPG, Ponta Grossa. 526 p.
- Martins CR, Hay JDV, Walter BMT, Proença CEB & Vivaldi LJ (2011) Impacto da invasão e do manejo do capim-gordura (Melinis minutiflora) sobre a riqueza e biomassa da flora nativa do Cerrado sentido restrito. Brazilian Journal of Botany 34: 73-90.
- Martorell C & Peters E (2009) Disturbance- response analysis: a Method for rapid assessment of the threat to species in disturbed áreas. Conservation Biology 23: 377- 387.
- Melo MS, Moro RS & Guimarães GB (2014) Patrimônio natural dos Campos Gerais. UEPG, Ponta Grossa. 233p.
- Méndez M, Durán R Olmsted I & Oyoama K (2004) Population dynamics of Pterocereus gaumeri, a rare and endemic columnar cactus of Mexico. Biotropica 36: 492-504.
- Ménezes OT & Silva SR (2015) Cactaceae do Ceará, Brasil: prioridades para a conservação, Ceará. Gaia Scientia 9: 67-76.
- Moro RS & Carmo MRB (2014) A vegetação Campestre nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 93-98.
- Neto PHW & Rocha CH (2014) Caracterização da produção agropecuária e implicações ambientais nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio natural dos Campos Gerais do Paraná. Ed. UEPG, Ponta Grossa. Pp. 182-190.
- Oliveira JPL de (2009) Ecologia de Discocactus zehntneri subsp. boomianus (Cactaceae) em afloramento rochoso do semi-árido baiano (Brasil) Dissertação de Mestrado. Universidade Federal da Bahia, Salvador. 100p.
- Ortega BP & Godínez ÁH (2006) Global diversity and conservation priorities in the Cactaceae. Biodiversity and Conservation 15: 817-827.
- Ortega BP, Suring S, Sajama J, Sotola E, Alonso PM, Bravo S & Godínez AH (2010) Diversity and conservation in the Cactus family. In: Ramawat KG (ed.) Desert plants: biology and biotechnology. Springer, New York. Pp 157-173.
- Pickering CM & Hill W (2007) Impacts of recreation and tourism on plant biodiversity and vegetation in protected areas in Australia. Journal of Environmental Management 85:791-800.
- Pimm SL, Russell GJ, Gittleman JL & Brooks TM (1995) The future of biodiversity. Science 269: 347-350.
- Ribeiro EMS (2011) Influências de perturbações antrópicas sobre população de Cactaceae em áreas de Caatinga. Dissertação de Mestrado. Universidade Federal de Pernambuco, Recife. 67p.
- Ricklefs RE (2010) A economia da natureza. Ed. Guanabara, Rio de Janeiro. 572p.
- Rocha CH & Neto PHW (2014) Origens dos sistemas de produção e fragmentação da paisagem nos Campos Gerais. In: Melo MS, Moro RS & Guimarães GB (eds.) Patrimônio Natural dos Campos Gerais do Paraná. Ed. UEPG, Ponta Grossa. Pp. 171-180.
- Sá MFM (2014) Solos. In: Melo MS, Moro RS & Guimarães GB Patrimônio Natural dos Campos Gerais do Paraná. UEPG, Ponta Grossa. Pp 73-83.
- Salazar CRL & Moreira NM (2019) Nuevo registro de Melocactus peruvianus (Cactaceae) y estado de conservación del género Melocactus en el Ecuador. Rodriguésia 70: 2-9.
- Santos MR. & Oliveira ATF (2008) Influência de variáveis ambientais e espaciais na distribuição geográfica da família Cactáceae no Leste do Brasil (Proyectos). Boletín de la Sociedad Latinoamericana y del Caribe de Cactáceas y otras Suculentas 5: 5-6.
- Sema (2018) Conhecendo o bioma Mata Atlântica. Revista Atlântica 1: 1-20.
- Silva SR, Zappi D, Taylor N & Machado M (2011) Plano de ação nacional para conservação de Cactáceas. Instituto Chico Mendes de Conservação da Biodiversidade, Brasília. 58p.
- Soller A, Soffiatti P, Calvente A & Goldenberg R (2014) Cactaceae no estado do Paraná, Brasil. Rodriguésia 65: 201-219.
- Steenbergh WE & Lowe CH (1977) Ecology of the saguaro: II, Reproduction, germination, establishment, growth, and survival of the young plant. Department of the Interior, National Park Service Scientific Monograph Series, Washington. 226p.
- Tapia RC, Mandujano MC, Valverde T, Mendoza A & Freaner FM (2005) How important is clonal recruitment for population maintenance in rare plant species? The case of the narrow endemic cactus, Stenocereus eruca, in Baja California, México. Elsevier Science 125: 123-132.
- Taxonline Rede Paranaense de Coleções Biológicas. Available at <https://taxonline.bio.br/index.php> . Access on 23 April 2020.
» https://taxonline.bio.br/index.php - Zappi D & Taylor N (2020) Cactaceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available at <http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB70>. Access on 29 September 2020.
» http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB70 - Ziller SR, Galvão FA (2002) A degradação da estepe gramíneo-lenhosa no Paraná por contaminação biológica de Pinus elliottii e P. taeda Floresta 32: 41-47.
- Zuur AF, Leno EN & Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1: 3-14.
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Publication Dates
-
Publication in this collection
03 Dec 2021 -
Date of issue
2021
History
-
Received
25 June 2020 -
Accepted
15 Jan 2021