Drought changes fruiting phenology, but does not affect seed predation of a keystone palm

Highlights

• Plant flowering and fruiting patterns are influenced by temperature and rainfall.

• Drought decreases flower and seed production in the palm Syagrus romanzoffiana.

• Seed predation is similar between periods of regular rainfall or drought.

• Climate change increases drought frequency and may impair palm regeneration.

Abstract

Climate change models predict an increase in frequency, intensity, and duration of extreme climatic events, such as severe droughts. These changes can influence plant reproductive phenology, with potential delayed consequences for plant regeneration and could impact plant-animal interactions. One of the possible responses to these changes in phenology is the modification in crop size, which can further impact seed predation, dispersal and plant recruitment. However, plant responses to droughts and their cascading consequences for animals are still poorly described for tropical species. Here, we evaluated whether phenology and seed predation of a keystone palm (Syagrus romanzoffiana) are influenced by droughts in the Atlantic Forest from southeastern Brazil. We recorded the reproductive phenology and the predation of seeds fallen beneath palms in forest fragments for 4 years, comparing periods impacted by severe droughts to periods of regular rainfall. Flowering and fruiting patterns were correlated with climatic variables, especially temperature and rainfall. The number of bunches with flowers or ripe fruits decreased in periods of drought. Drought also changed the seasonal patterns of reproductive phenology when compared with regular rainfall periods, anticipating flowering and delaying unripe fruit occurrence. Weevils and rodents shifted roles in seed predation among years, irrespective of droughts. Our results indicate that drought affects reproductive phenology of this keystone palm and may compromise plant regeneration. Droughts, however, produce no clear cascading effect on predation of seeds fallen beneath parental plants.

Introduction

Understanding species responses to climatic variables is important to predict the effects of climate change in the biology of organisms and their interspecific interactions (Morellato et al., 2016). Over the past decades, several species experienced changes in abundance and reductions in their range due to climate change (IPCC, 2019; Thuiller, 2004; Wilson et al., 2005; Van der Putten et al., 2010). Species phenology, i.e., the periodic events in the life of living beings and their correlations with climate variations, has been considered an important tool to interpret the effects of climate change on animals and plants, as well as in predictive models of future scenarios with higher temperatures (Parmesan, 2006; Memmott et al., 2007). However, information about plant phenology over the years is still scarce in most tropical and subtropical regions (Mendoza et al., 2017).

Climate change will probably lead to an increased duration, frequency, and intensity of extreme events, such as droughts, floods, and storms (IPCC, 2019). In addition, it could lead to an extension of the dry season in some tropical areas, and consequently to the shortening of the wet season, with implications for plant phenology (Morellato et al., 2016). There is an expectancy of an increased frequency of events such as El Niño Southern Oscillation (ENSO), which can cause precipitation anomalies in southern Brazil (Cai et al., 2020), where there are some of the largest remnants of the threatened and biodiversity rich Atlantic Forest (Ribeiro et al., 2009). Tropical tree responses to drought vary from changes in photosynthesis and leaf investment to changes in seasonality of plant phenology, acclimation or death, among others (Domingues et al., 2018), including a reduction in flowering and fruiting of at least some species (Brando et al., 2008). Since plant reproduction in the tropics is often closely correlated with rainfall precipitation, changes in total rainfall and seasonality could alter reproductive patterns of many species, with possible cascading effects to other trophic levels since fruits and seeds are important food resources for most vertebrates in the tropics (Butt et al., 2015).

Among-plant variations in seed crops may also affect seed predation rates. Seed predators may show a positive density-dependence response and destroy an increasing number of seeds from more productive plants during pre- (Francisco et al., 2008) and post-dispersal seed predation (Wang, 2019). However, high seed density may also decrease the proportion of seeds lost to granivores. Great temporal variations in seed crops may not sustain permanently large populations of a seed predator that show high specificity for that seed species; as a result, in years of high seed crops (e.g. masting) small granivore populations will be satiated and more seeds would escape predation (Janzen, 1971; Kelly, 1994; Wang, 2019; Bogdziewicz et al., 2020). Studies investigating changes in plant phenology due to climate change, and their consequences for animals that interact with these species are still rare and are showing no obvious responses. For example, an increase in temperature caused by climate change induces greater regularity in seed production over the years of the European mast seeding tree Fagus sylvatica, which could be interpreted as beneficial to plant recruitment (Bogdziewicz et al., 2020). However, the regular supply of F. sylvatica seed resources every year increased rodent abundance permanently, resulting in much higher and regular seed predation rates, which is capable of limiting plant recruitment (Bogdziewicz et al., 2020). The once successful predator satiation strategy of F. sylvatica is no longer working in a scenario of climate change (Bogdziewicz et al., 2020).

The availability of fleshy fruits usually decreases in the dry season in the Atlantic Forest (Genini et al., 2009; but see Morellato et al., 2000). In Central America, severe droughts caused by ENSO can decrease fruit availability, leading to an increased mortality of frugivores (Wright et al., 1999). Scarcity of food resources can also turn seed dispersers into seed predators, leading to a disruption of mutualistic interactions (Jorge and Howe, 2009). Therefore, the impacts of climate change in long-term species persistence will probably depend on how species will respond to such changes, as well as the effects on interspecific interactions (Morellato et al., 2016; Bogdziewicz et al., 2020).

Palms are considered keystone species to frugivores due to the high fruit production that supports a broad range of animals that consume their fruits and seeds (e.g., frugivorous vertebrates), especially in periods of fruit scarcity (Terborgh, 1986; Genini et al., 2009). In the Atlantic Forest, the palm Syagrus romanzoffiana provides fruits for at least 60 vertebrate species (Mendes et al., 2015). Larvae of weevils, such as Revena rubiginosa (Coleoptera: Curculionidae), feed on seeds of S. romanzoffiana and rely totally on them to complete their life-cycle (Alves-Costa and Knogge, 2005). S. romazoffiana seems to produce fruits during the whole year and is crucial for the local fauna, especially during the dry season, being considered a keystone species (Mendes et al., 2015; Genini et al., 2009). Changes in abiotic conditions due to habitat fragmentation and edge effects enhance seed production in some palms from the Atlantic Forest, increasing the likelihood of recruitment (Andreazzi et al., 2012).

Understanding the responses of the phenology of S. romanzoffiana to climate change (represented by droughts) and their potential cascading effects to seed predation can help us to predict potential implications for plant recruitment and fauna. Thus, the main aims of this paper were: (i) to investigate the response of S. romanzoffiana reproductive phenology to changes in climatic variables, including periods of drought; (ii) to assess the effect of drought on seed predation rates and test if large seed crops lead to satiation of seed predators. We expect that drought induces changes in the timing of flowering and fruiting and decreases the number of reproductive bunches in S. romanzoffiana, leading to high levels of seed predation compared to years of regular rainfall.