Open-access Unraveling fruit and seed morphology and seedling establishment of a narrow endemic tree species

Desentrañando la morfología de frutas y semillas, así como el establecimiento de plántulas de una especie de árbol estrechamente endémica

Abstract

Montane ecosystems in South America harbor high levels of endemism typically with species that are often threatened. Here we investigated fruit and seed morphology, germination, and early growth parameters of Crinodendron brasiliense, an endangered and narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. We obtained fruit and seed size and shape, number of lobes and number of seeds per fruit and evaluated germination and early growth parameters in a greenhouse. We tested the effect of different container types and parent plant on seed morphology, germination, and early growth. We also tested whether thermal scarification would improve germination rates. We showed that parent plant significantly influenced fruit and seed morphology as well as early growth rates. The germination rate of the species was extremely low (0.003–0.004 seeds per day), which may be one important underlying cause of its small population size and restricted distribution. Thermal scarification was ineffective to improve the germination of seeds. Unexpectedly, container type significantly affected germination success, as seeds in trays germinated faster and in higher rates than seeds planted in seedbeds. Such result suggests a higher soil moisture could improve germination success. Our study is the first documented propagation of the species and provides essential aspects on the reproductive biology and early development of Crinodendron brasiliense. We highlight the urgent need for further research and collaborative conservation initiatives to prevent the extinction of this species.

Keywords Araucaria Forest; Brazil; Cloud Forest; Conservation; Crinodendron brasiliense; Elaeocarpaceae; Montane Forest

Resumen

Investigamos la morfología de frutos y semillas, la germinación y los parámetros del crecimiento inicial de Crinodendron brasiliense, una especie arbórea en peligro de extinción y endémica de los bosques montanos del sur de Brasil. Obtuvimos el tamaño y la forma de frutos y semillas, el número de lóbulos por fruto y el número de semillas por fruto, además de evaluar los parámetros de germinación y crecimiento inicial – desconocidos para la especie. Demostramos que la planta madre influyó significativamente en la morfología de frutos y semillas, así como en las tasas de crecimiento inicial. La tasa de germinación de la especie fue extremadamente baja (0.003–0.004 semillas por día), lo que podría ser una causa importante para explicar su pequeño tamaño poblacional y restringida distribución. La escarificación térmica fue ineficaz para la germinación de semillas. Inesperadamente, el tipo de contenedor afectó significativamente el éxito de la germinación, ya que las semillas plantadas en bandejas germinaron más rápido y en tasas más altas que las semillas plantadas en semilleros. Tal resultado sugiere que una mayor humedad del suelo podría mejorar el éxito de la germinación. Nuestro estudio es el primer registro documentado de la propagación de esta especie y proporciona aspectos esenciales sobre la biología reproductiva y el desarrollo inicial de Crinodendron brasiliense. Destacamos la necesidad urgente de realizar más estudios e iniciativas de conservación colaborativas para evitar la extinción de esta especie.

Palabras clave Bosque con Araucária; Bosque montano; Bosque nuboso; Brasil; Conservación; Crinodendron brasiliense; Elaeocarpaceae

Introduction

Narrow endemic species are those with a very limited geographic range, usually restricted to a specific area or habitat (Strayer 2013, Behroozian et al. 2020). These species are often vulnerable to extinction due to their restricted distribution and low population sizes, making them a conservation concern (Kier et al. 2009). Narrow endemic species are typically found in isolated habitats such as mountaintops, islands, or isolated valleys, and they are often highly adapted to the specific conditions of such environments (Lavergne et al. 2004, Nogué et al. 2013). Montane ecosystems in South America, such as the Andes (e.g., (Aagesen et al. 2012), the Guyana Highlands (e.g., (Nogué et al. 2013), and the Brazilian Subtropical Highlands (e.g., (Werneck et al. 2011, Iganci et al. 2011, Hassemer et al. 2015), harbor high levels of endemism, especially plants. High endemism in such ecosystems can result from speciation rates associated to topographical isolation (Steinbauer et al. 2016). Local persistence is also a key feature of narrow endemics survival, once they tend to be poor competitors and less tolerant to stress or disturbance than widespread species (Lavergne et al. 2004). Because of their limited range, narrow endemic species are threatened by disturbances such as wildfires, landslides, stressors such as droughts, as well as human-induced impacts such as habitat destruction and fragmentation, and climate change (Essl et al. 2009, Dirnböck et al. 2011, Hassemer et al. 2015). As such, to ensure their survival, endemic species require special conservation efforts, such as habitat protection and restoration including human-assisted propagation (Toledo-Aceves 2017). Thus, understanding biological and ecological aspects of narrow endemic species is essential for developing conservation strategies to prevent their extinction (Lavergne et al. 2004).

Critical stages in the life cycle of plants such as germination and early growth play a crucial role in population stability and ecological interactions. The comprehension of which and how much factors influence both stages is essential, as they can determine success or failure of a plant species (Miller et al. 2017) and population dynamics (Buckley et al. 2010). Soil fertility, temperature, water availability, and light intensity are among the main factors that impact the germination and early growth of plants (Bareke 2018). Besides, genetic factors can as well affect germination parameters, such as percentage of and time for germination (Bischoff et al. 2006). In addition, understanding early development stages can provide insights into the adaptive strategies employed by plants to cope with environmental challenges and can help predict how plant communities may respond to future environmental changes (Fay & Schultz 2009, Buckley et al. 2010). Therefore, the investigation of germination and early growth stages are critical aspects of ecological research that can inform conservation, restoration and management of plant populations and communities.

Crinodendron (Elaeocarpaceae) is a plant genus endemic to South America and with just four described species: Crinodendron brasiliense Reitz & L. B. Sm. (found only in Southern Brazil), Crinodendron hookerianum Gay (found only in Chile), Crinodendron patagua Molina (found only in Chile) and Crinodendron tucumanum Lillo (found in Argentina and Bolivia) (Bricker 1991, Blundo et al. 2012). Crinodendron brasiliense is the narrowest endemic species of its genus and occurs in a very limited geographic range in subtropical montane cloud forests in Southern Brazil (Bricker 1991, Sühs 2018, Sampaio 2020). Although described as a shrub up to 4 meters in height, it can reach up to 12 meters in height and thus be considered a tree (Sühs et al. 2019). Leaves are glossy, dark green in color and pendulous; flowers are bell-shaped and white in color (Smith & Smith 1970, Bricker 1991). Any information about the species’ fruit and seed morphology, cultivation or propagation studies are still missing. Besides being narrow and endemic, C. brasiliense is currently classified as an “endangered” species by the International Union for Conservation of Nature standards (IUCN – Sühs 2018). It faces multiple threats, including habitat destruction, fragmentation, climate change, as well as a low known population size of < 250 adult individuals (Sühs 2018). Therefore, conservation efforts, such as habitat protection and management, in addition to basic research on biological and ecological aspects are needed to ensure the survival of this species and develop effective conservation strategies.

Biological and ecological data are crucial for the development of solid and integrated conservation programs for narrow endemic and endangered species (Lavergne et al. 2004). Considering that aspects on fruit and seed morphology, germination and early growth stages are currently unknown for the narrow endemic and endangered plant Crinodendron brasiliense, which are paramount for the perpetuation of the species, we aimed to examine fruit and seed morphology, determine germination rate and early growth parameters. We measured fruit and seed size and shape, number of lobes per fruit and number of seeds per fruit from several individuals and developed a greenhouse experiment to test germination and monitor early growth development. Such new data allowed us to answer the following questions: Does parent plant affect fruit and seed morphology? Does thermal scarification improve the germination of C. brasiliense? Does container type affect germination of C. brasiliense? Does parent plant identity affect early growth of C. brasiliense? By answering these questions and achieving the proposed goals, we believe some crucial ecological and biological information can be available, providing means for the development of conservation initiatives for this narrow endemic species.

Material and Methods

1.

Study area

This study was conducted in the highlands of southern Brazil, in both the São Joaquim National Park (SJNP) and its surroundings. SJNP is a protected area with 49,500 hectares which protects Araucaria forests, cloud forests, highland grasslands, and subtropical evergreen forests. Crinodendron brasiliense is found in this region, in Araucaria forests / montane cloud forests, mainly in altitudes above 1500 m a.s.l. (Sühs et al. 2019). The climate between 2007 and 2020, recorded in the nearest weather station (ca. 30 km), was characterized by an annual mean rainfall of 2,822.3 mm yr–1, equally distributed along the year, and an annual mean temperature of 11.1°C. The average minimum temperature for the coldest month (July) was 7.7°C and the average maximum temperature for the hottest month (January) was 14.3°C (INMET- inmet.gov.br).

2.

Data collection

2.1.
Fruit and seed morphology

Adult individuals (hereafter: parent plant) of Crinodendron brasiliense found in previous surveys and field incursions were selected based on the presence of fruits. All individuals were located within or close to the extent of the SJNP, above 1500 m a.s.l. and were no further than 8 km from each other, thus likely belonging to the same population or meta-population. We collected a minimum of 20 ripe fruits from 17 parent plant of C. brasiliense between January 29th and February 6th, 2022. A total of 362 fruits were collected and 350 fruits were selected for measurements. In each fruit, we measured length and width and the number of lobes and seeds per fruit was counted. Open fruits were not measured in length and width. We manually extracted seeds from the fruits and then screened them for maturity, where green seeds were considered immature and brown seeds were considered mature. A total of 350 mature seeds were selected for measurements, proportionally to the number of fruits used for each plant. We calculated fruit and seed shape and size. Shape was considered as the ratio between length and width and size was considered as the product between length and width (e.g., (Dong et al. 2023). Seeds were kept separated by parent plant and were kept refrigerated until seeding.

2.2.
Germination

Mature seeds were sown at a depth of two centimeters in two container types, seedbeds, and trays, containing a mixture of inert substrate and sand, in a proportion of 3 to 1, respectively. We sow 128 seeds in each seedbed, in a total of 16 seedbeds; and 36 seeds in each tray, in a total of 6 trays. The total number of seeds was 2,264 seeds, of which 2,048 were sown in seedbeds and 216 in trays. The main difference between the two containers was that trays held a larger volume of substrate, thus retaining more moisture compared to the seedbeds. The total number of seeds collected per individual was divided into two treatments: a thermal scarification treatment (“thermal scarification”) and a control treatment without scarification (“control”). For the thermal scarification, we immersed seeds in hot water (~90°C) for 60 seconds (Gray 1962). Seeds from both treatments were placed to germinate in the same seedbeds/trays. The trays and seedbeds were numbered and identified with metal tags. We keep track for each individual seed regarding the treatment, and parent plant it came from. The experiment was conducted in an open nursery with 50% shade cloth on top, on 1.5 meters high benches to prevent seed predation. The seeds were planted on 08/02/2022 with subsequent watering. During the first week, containers received daily watering, and thereafter, watering was done every 3 days. The location of seedbeds and trays was randomized in the nursery every 2 months. The germination percentage and germination time were calculated for each treatment. The duration of the germination experiment from the planting date (08/02/2022) to the end date (17/02/2023) was 374 days. We considered as germination success the emission of a cotyledon. We considered germination speed as the time needed to germinate. No seeds from the thermal scarification treatment germinated; therefore, these data were not included in the analysis. Also, 60 seeds from the control were lost for unknown causes but are unlikely to bias our results.

2.3.
Early growth

When seedlings developed their third pair of true leaves (48 ± 11 days after germination), they were transplanted into individual 1.5 L pots. Once transplanted, seedlings were watered every two days for a period of 10 days. There were no subsequent waterings as rainfall was regular throughout the experiment period. Randomization of the location of pots was done monthly. We considered the height of the seedling/sapling as a parameter for initial growth. Initially, seedlings were measured every 15 days, and later at a monthly basis. The duration of the early growth experiment from the first transplanting date (14/12/2022) to the end date (31/05/2023) was 168 days. General aspects of the plant regarding flowers, fruits and seeds, seedling germination, seedling development, and habitat can be found in Figure 1 (A to F, respectively).

Figure 1
General aspects of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. A: flowers; B: fruit with exposed seeds; C: seedling germination; D: seedling development; E: subtropical montane cloud forest (interior); and F: subtropical montane cloud forest/ Araucaria Forest (exterior).
3.

Data analysis

We evaluated fruit and seed morphology by modelling fruit and seed shape and size as a function of the parent plant. For fruit shape and size and seed size, we used generalized linear models (GLM) with a gaussian distribution because it fit the data better. For seed shape we used the Gamma distribution and log-transformed the seed shape data. Descriptive statistics for the whole data set were as well provided. To test the effect of different containers (seedbeds/trays) on the germination success (odds) of Crinodendron brasiliense, we used generalized linear mixed models (GLMM) with a binomial distribution, using the logit link function. We included the container nested with parent plant as a random effect variable. All models were selected by Akaike Information Criterion (AIC) by comparing models with fixed effects to an intercept-only model.

The germination parameters of germination percentage, peak germination time, mean germination rate and germination speed were calculated separately for each container type and described. We considered germination speed as the rate of germination in terms of the total number of seeds that germinate in a time interval (Aravind et al. 2023). We fit a GLMM to model plant height over time (for individuals with at least 6 measurements over time). Time was considered as days after germination. We used a gaussian distribution because it fit the data better and included the parent plant as a fixed effect term in the model. Since very few seeds germinated, only five parent plants (out of the 17) were kept for this model. The individual was included as a random effect term in the model (following recommendations of Paine et al. 2012).

All models were validated by means of residual evaluation. We assessed goodness-of-fit of the produced models through loglikelihood ratio pseudo-R2. Analyses were calculated in R environment (R Core Team 2020), through the packages ‘germinationmetrics’ (Aravind et al. 2023) for calculating germination parameters, glmmTMB (Magnusson et al. 2020) for GLMM model, DHARMa (Hartig 2016) for model validation, MuMIn (Barton 2009) for goodness-of-fit, visreg (Breheny & Burchett 2017) for model visualization and ggplot2 (Wickham 2016) for data visualization.

Results

1.

Fruit and seed morphology

Fruit length and width had similar values and varied between 1.0 cm to 3.1 cm in length and between 1.2 cm to 3.3 cm in width. The mean number of lobes per fruit was 3 (standard deviation – SD ± 0.4) and the mean number of seeds per fruit was 3.6 (SD ± 1.6). Seed length and width values were similar, with mean length of 0.5 cm (SD ± 0.04) and mean width of 0.4 cm (SD ± 0.04; Table 1). Further measurements can be found in Table 1.

Table 1
Summarized values of fruit and seed morphology of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. N = sample size, MAD = median absolute deviation, SD = standard deviation, Min = minimum value and Max = maximum value.
1.1.
Does parent plant affect fruit and seed morphology?

Yes. The shape and size of both fruits and seeds varied according to the parent plant to which they belonged (Figure 2). The parent plant explained 35% of the variation in fruit shape and 56% of the variation in fruit size. The mean fruit shape (length/width) was 0.9 cm (SD ± 0.13), and the mean fruit size (length*width) was 4.9 cm (SD ± 1.5) (Table 1). The parent plant explained 32% of the variation in seed shape and 42% of the variation in seed size. The median seed shape (length/width ratio) was 1.3 cm (median absolute deviation – MAD ± 0.14), and the mean seed size (length*width) was 0.2 cm (SD ± 0.03) (Table 1). All models performed better than the intercept-only model and were considered valid through residual inspection. Numeric results of all models are presented in Supplementary Information – Table S1.

Figure 2
GLMM model results for evaluating the effect of parent plant on fruit and seed morphology of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. A and B represent shape (length/width ratio) and size (length * size) of fruits, respectively; C and D represent shape and size of seeds, respectively. Boxplots not sharing any letter are significantly different (Tukey test at the 95% level of significance). A violin plot with all sampled values (black dots) is displayed in the right of each graph. The red dot indicates the mean (A, B and D) and median (C); red lines indicate standard deviation (A, B and D) and median absolute deviation (C).
2.

Germination

2.1.
Does hot water seed scarification improve the germination of C. brasiliense?

No. Seeds scarified with hot water did not germinate (therefore we do not present any further result regarding this question).

2.2.
Does container type affect germination of C. brasiliense?

Yes. Seeds sown in trays had a greater chance to germinate than seeds sown in seedbeds (z = 3.98, p < 0.001). The odds of a seed to germinate in trays were 36 times greater than the odds of a seed to germinate in seedbeds. The odds for a seed to germinate in seedbeds was 0.0028, while the odds for a seed to germinate in trays was 0.1016 (Figure 3). The produced model explained 19% of data variation (pseudo-R2 theoretical variance = 0.188).

Figure 3
Germination success (odds) for seeds of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil, sown in seedbeds and trays. Different letters indicate significantly different results between groups (Binomial GLMM at 95% level of significance).
2.3.
Germination parameters

A total of 31 seeds from the control group germinated (2.9% of 1,071 seeds). Seeds planted in trays germinated faster (Figure 4) and in a higher rate than seeds sown in seedbeds. The germination parameters of germination percentage, peak germination time, mean germination rate and germination speed were calculated separately for each container type and are described in Table 2.

Figure 4
Cumulative germination curves of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. Grey color indicates seeds sown in seedbeds and orange color indicates seeds sown in trays.
Table 2
Germination parameters of Crinodendron brasiliense in an experiment conducted in an open nursery, Southern Brazil.
3.

Early growth

3.1.
Does parent plant affect early growth of C. brasiliense?

Yes. The height of seedlings varied according to the parent plant to which they belonged (Figure 5A). The produced model with parent plant and number of days after germination (Figure 5B) as fixed effects explained 78% of data variation (marginal pseudo-R2 = 0.78, conditional pseudo-R2 = 0.88).

Figure 5
GLMM model results for evaluating the effect of parent plant (A) and time (B) on seedling height of Crinodendron brasiliense, a narrow endemic tree species of subtropical montane cloud forests in Southern Brazil. Boxplots not sharing any letter are significantly different (Tukey test at the 95% level of significance).

Discussion

Beyond showing basic aspects on the morphology of fruits and seeds, we found that the parent plant plays an important role in fruit and seed morphology by affecting shape and size of fruits and seeds. Thermal scarification of seeds was completely ineffective to improve germination of the species, possibly indicating that when passing through the digestive tract, particularly of large animals, seeds will not germinate. Seeds planted in trays germinated faster and in a higher rate than seeds sown in seedbeds, suggesting higher success rates when using containers that retain more moisture. Parent plant also influenced the development of the individuals by affecting seedling height in early growth development stage.

1.

Fruit and seed morphology and early growth

We found parent plant played a significant role in fruit and seed morphology (shape and size of fruits and seeds) as well as in early growth. Such intraspecific variation was unexpected, especially considering that individuals likely belong to the same population, occur in very similar environmental conditions, and were planted within similar conditions of soil and light availability. In general, intraspecific variation in fruits and seeds can occur across gradients (e.g., Guja et al. 2014) and across spatial scales (e.g., Cavazos 2022). This variation can be a result of genotypic variations and phenotypic plasticity (Cavazos 2022), likely triggered by environmental factors or biotic interactions (Herrera 1992, Albert et al. 2010, Johnson et al. 2019). Intraspecific variations in fruit and seed morphology and in early growth can influence both dispersal mechanisms and fitness, affecting the species’ overall reproductive success and population dynamics (Buckley et al. 2010, Galetti et al. 2013, Johnson et al. 2019). Since parent plant was important to explain fruit and seed morphology as well as seedling development, we strongly recommend future studies to consider evaluating genetic diversity (e.g., Xu et al. 2016) and whether fruit and seed morphology can affect dispersal and development of the species.

2.

Germination

The unsuccessful germination of seeds subjected to thermal scarification reveals the inefficacy of this technique for enhancing germination in C. brasiliense. This result was not a surprise given that C. brasiliense seeds lack a rigid coat or any hard structure that could require scarification or interruption of dormancy. Still, the fact that none of the seeds germinated after the thermal scarification suggests germination will unlikely improve with scarification methods applied for similar purposes (such as immersion in sulphuric acid; Gray 1962). This result possibly applies for other Crinodendron species that share similar seed structure (Bricker 1991). Although germination was higher in trays than in seedbeds, the germination rate of C. brasiliense can be considered extremely low compared to other unrelated species from tropical montane forests in Mexico (Toledo-Aceves 2017), Brazil (Dos Santos et al. 2023), and Colombia (Vásquez et al. 2012). Considering both the low germination rate and the long-time seeds took to reach peak germination (246 days – 8 months), we believe the low population size of Crinodendron brasiliense can be a consequence of recruitment failure (Volis 2019). Moreover, the temperature fluctuations spanning from fruit-ripening in summer, passing by the cold and frosty winter, until seed germination in spring can be important for the species. It is thus possible that the species’ germination can occur after exposure to a cold period, thus benefiting from a cold stratification treatment. Besides temperature, moisture levels also seem to be important. We showed a strong effect of container type on germination rates underscores the importance of substrate moisture retention provided by container volume, suggesting that container choice during propagation can be crucial to improve germination success rates and plant development (NeSmith & Duval 1998). These results are particularly relevant for species propagation efforts. We recommend propagating C. brasiliense by carefully extracting seeds from fruits and directly sowing them into individual containers capable of retaining good amounts of moisture. These containers should have a minimum volume of 1.5 liters of soil, and precautions should be taken to prevent the soil from becoming excessively dry. Also, future studies could investigate whether a cold stratification treatment could trigger germination of C. brasiliense and the causes of a possible recruitment failure.

3.

Conservation implications

Species with limited distribution and small population sizes, such as narrow endemic species, usually rely on local persistence for survival (Lavergne et al. 2004), are often at risk of extinction (Essl et al. 2009), and require priority conservation efforts (Kier et al. 2009, Hassemer et al. 2015). Consequently, safeguarding the existence of endemic species demands conservation measures, such as species monitoring and management (Robinson et al. 2018), including human-assisted propagation in some cases. To meet conservation goals, it is crucial to know basic aspects on the biology of the species. In this sense, our study provides new and important insights into the biology and ecology of Crinodendron brasiliense – most if not all information previously unknown. By addressing questions related to fruit and seed morphology, germination and early growth, our findings contribute to the understanding of the species biology and marks the first investigation directed to this species and the first documented propagation of the species. This achievement not only sheds light on important aspects of the species’ life cycle but also holds profound significance for enhancing its persistence and survival. Our effort lays a foundation for future programs aimed at increasing the population size of C. brasiliense (e.g., Volis 2019), underscoring its importance for conservation initiatives and biodiversity conservation (Toledo-Aceves 2017). Conservation of montane cloud forests, the main habitat in which C. brasiliense occur, are also extremely important. Despite being within a protected area (São Joaquim National Park), Crinodendron populations are threatened by wildfires that occur mainly because of fire exclusion in adjacent grasslands (Sühs et al. 2020). Therefore, controlled fire in grasslands can be considered to prevent montane cloud forests from burning with wildfires.

Considering the small distribution range and the extinction risk status (Sühs 2018), Crinodendron brasiliense still lacks dedicated conservation programs, and there are no active propagation efforts in place. The absence of C. brasiliense from the list of threatened plants in its home-state (State of Santa Catarina, Brazil), as of the last update in 2014, underscores the urgency for a more recent assessment to accurately determine and address its current conservation status. Consequently, the species is still unknown to many authorities, conservationists, and non-specialists. Thus, urgent attention and concerted efforts are required to address the critical conservation needs of this species.

This study provides essential aspects on the reproductive biology and early development of Crinodendron brasiliense and highlights the urgent need for future research and collaborative conservation initiatives. We appeal to the scientific community, conservation managers, and the general population to join forces in developing targeted strategies to ensure the survival and long-term sustainability of this narrow endemic and endangered plant species.

Supplementary Material

The following online material is available for this article:

Table S1 - Models produced to evaluate the effect of parent plant (C1:C21) on fruit and seed morphology of Crinodendron brasiliense, a narrow endemic tree species of southern Brazilian highlands. CI = confidence interval. Note that the P-Values provided changed after adjustment for multiple comparison tests.

Acknowledgments

We thank the Instituto Chico Mendes de Conservação (ICMBio) and managers of São Joaquim National Park for allowing the research to be performed. We thank Elisson José Machado, for the field assistance. We appreciate the logistical and financial support from the Long-Term Ecological Research Program - Biodiversity of Santa Catarina (LTER-BISC).

The present work was supported by the CNPq/MCTI/CONFAP-FAPS/PELD nº 21/2020 and FAPESC/2021TR386. RBS received financial support from CNPq (PELD 2020, process 163412/2021-9); SC received financial support from CNPq (PELD 2020, process 156930/2021-8); SKN received financial support from CNPq (PELD 2020, process 441990/2020-7); and JS received financial support from CNPq (PELD 2020, process 114319/2023-5).

Data Availability

Supporting data are available at <https://doi.org/10.5281/zenodo.10664507>.

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Edited by

  • Associate Editor
    Carlos Joly

Publication Dates

  • Publication in this collection
    02 Aug 2024
  • Date of issue
    2024

History

  • Received
    15 Feb 2024
  • Accepted
    02 July 2024
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E-mail: contato@biotaneotropica.org.br
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