Phenological cycles in the Pantanal woody communities: Responses to climate and soil moisture seasonality

pushing natural ecosystems in tropical regions to tipping points with loss of resilience [1]. Compared with South American upland rainforests, floodplains and riparian wetlands are among the most important inland wetlands in terms of the ecosystem services provided to peo- ple; vegetation composition and function are directly linked to the services provided, such as nontimber products, erosion control, carbon sequestration, and habitats for species [2–5]. Covering approximately 20% of South America, more than 2 million km2 [6], the extent of nat- ural wetlands continues to decline, and insufficient information on the state and impacts from human activities limits their protection [7,8]. In floodplain wetlands, cyclic biological events in plants, such as leaf fall, flowering, fruiting, and seed germination, are indicators of plant functional strategies and often differ along soil hydrological gradients [9,10]. Flood timing and predictability are influenced by seasonal cli- mate rhythms and are the primary drivers of plant species zonation, assemblages, and season- ality of ecosystem productivity [11–14]. Species adaptations to the flood cycle vary widely: some tree species exhibit dormancy followed by leaf fall during flooding, whereas some ever- green trees tolerate flooding by maintaining their metabolism and leaves [15]. The end of the wet season is known to trigger the production of new leaves and fruits on deciduous plants, whereas for evergreen species, sclerophyllous foliage is an adaptive trait that reduces water loss

via transpiration. The synchronicity between seed dispersal and hydrology is another adapta- tion to the flood cycle, which may increase germination success [12]. Approximately 1,000 species of trees that are tolerant to different flood levels exist in Ama- zon floodplains [16]. In other extensive South American wetlands subjected to predictable monomodal flood pulses, such as the Pantanal Mato-grossense [17], the number of flood-toler- ant trees is much lower: approximately 355 species (47% of the Pantanal trees) [18]. Among the 2,567 known Pantanal flora [19], 756 species are classified as woody plants, representing 39.7% of the higher plants [18]. Unlike in the Amazon, the vegetation of the Pantanal is pre- dominantly savanna, with most trees inhabiting nonfloodable environments and being toler- ant to prolonged dry periods [18,20]. The Pantanal has a savanna climate with marked seasonality defined by a dry season for more than 5 months. In such a hyperseasonal savanna, as described by Eiten in 1982 [21], alternating dry and wet seasons might trigger the pheno- phase of the production of leaves, flowers, and fruits [22]. Savanna formations may undergo a high vapor hydric deficit that is 30% greater than that of forests in the dry season, affecting spe- cies water use, while some forests are more impacted by seasonal hydrological variation [23]. The capacity of habitats to store soil moisture during periods of low rainfall might provide humid microclimates to plants sensitive to drought [24]. The evolutionary response of species

to such seasonal water deficits may involve deep roots and stomatal or chemical control of water loss through evapotranspiration and leaf shedding [23,25]. As in other tropical wetlands [7,8], knowledge about the reproductive and vegetative cycles of woody plants in the Pantanal and their response to seasonality is insufficient [22], limiting our understanding of the func- tions of ecosystems and the impacts of human-induced environmental changes on biodiversity and ecosystem services. We do not yet know, for example, the impact of climate change on the Pantanal landscape composition and configuration, particularly under scenarios of 30% rain- fall reduction and up 7˚C temperature increase by 2100 [26]. Such changes could significantly affect the production of flowers and fruits, which are essential resources for some of the richest herbivore wildlife found in South America [27,28]. The intense wildfires of 2019–2020 in the Pantanal have challenged scientists in understanding the regeneration capability of plant com- munities, which might depend on the speed and direction of reproductive and vegetative phe- nological responses at the intra- and interspecific levels mediated by trade-offs in energy allocation for different parts of the plant [29]. PLOS ONE Phenological cycles in the Pantanal woody communities PLOS ONE | https://doi.org/10.1371/journal.pone.0316011 February 7, 2025 2 / 30 Funding: This work was funded by the Brazilian Science Council (CNPq) awarded to KLS and MIM, Brehm Foundation for International Bird Conservation, Germany, awarded to KLS, National

Institute for Science and Technology in Wetlands (INAU/ UFMT: www.inau.org.br), Brazil, awarded to KLS and MIM, and Instituto Arapyau´ awarded to the Science Panel for the Amazon, Brazil, JA. Competing interests: The authors have declared that no competing interests exist.