Disentangling the effects of foliar vs. floral herbivory of leaf-cutting ants on the plant reproductive success ofMiconia nervosa(Smith) Triana (Family Melastomataceae)

Abstract

Flower and leaf herbivory might cause relevant and negative impacts on plant fitness. While flower removal or damage by florivores produces direct negative effects on plant fitness, folivores affect plant fitness by reducing resource allocation to reproduction. In this study, we examine the effects of both flower and leaf herbivory by leaf-cutting ants on the reproductive success of the shrub species Miconia nervosa (Smith) Triana (Family Melastomataceae) in a fragment of Atlantic Forest in Northeast Brazil. We conducted a randomized block-designed field experiment with nine replicates (blocks), in which three plants per block were assigned to one of the three following treatments: undamaged plants (ant exclusion), leaf-damaged plants (ant exclusion from reproductive organs, but not from leaves), and flower + leaf-damaged plants (no exclusion of ants). We then measured flower production, fruit set, and fruit production. Our results showed that flower + leaf-damaged plants reduced flower production nearly twofold in relation to undamaged plants, while flower set in leaf-damaged plants remained constant. The number of flowers that turned into fruits (i.e., fruit set), however, increased by 15% in flower + leaf-damaged plants, while it slightly decreased in leaf-damaged compared to undamaged plants. Contrastingly, fruit production was similar between all treatments. Taken together, our results suggest a prominent role of ant floral herbivory across different stages of the reproductive cycle in M. nervosa, with no consequences on final fruit production. The tolerance of M. nervosa to leaf-cutting ant herbivory might explain its high abundance in human-modified landscapes where leaf-cutting ants are hyper-abundant.

Critical thermal limits in ants and their implications under climate change

“…Higher herbivory rates at higher temperatures could negatively affect plant performance (e.g. photosynthetic efficiency), especially if plants are subject to other stresses, such as those inhabiting forest edges, successional forests, or dry forests (Leal et al ., 2014; Tito et al ., 2016; Câmara et al ., 2020).…”

Divergent effects of leaf‐cutting ant herbivory and soil engineering on the reproductive success of plants in a Caatinga dry forest

“…Herbivores can impose severe damage to various plant parts, from roots to leaves and flowers, causing negative effects on plant reproductive success (Barber et al, 2015; Crawley, 1997; Lehtilä & Strauss, 1999; Maron, 1998; Poveda et al, 2003). These negative effects can either be caused by directly removing or damaging reproductive structures (i.e., flowers) or indirectly by removing photosynthetic or root tissues and suppressing the synthesis of assimilates, which can be invested in reproduction (Barber et al, 2015; Câmara et al, 2019; Cardel & Koptur, 2010; Lehtilä & Strauss, 1999; Tito et al, 2016). For instance, while pollination undeniably plays a pivotal role in fruit development (Ramírez & Davenport, 2013), herbivory can exert a notable influence.…”

“…A colony can consume between 70 and 500 kg of dry plant material per year (Herz et al, 2007), which can make up 15%–17% of the leaf production within their foraging areas and up to 50% of the local flora (as reviewed in Leal et al, 2014). Despite this widely recognised role of leaf‐cutting ants as key herbivores of neotropical ecosystems, there is only limited knowledge available about the fitness consequences of their harvesting activities at the single plant level (but see Câmara et al, 2019; Farji‐Brener & Tadey, 2017; Mundim et al, 2012). These few available studies on the effects of leaf‐cutting ant herbivory on plant reproduction report contrasting results with negative impacts on flower production (Câmara et al, 2019; Mundim et al, 2012), but also no effects on fruit set (Câmara et al, 2019; Farji‐Brener & Tadey, 2017).…”

“…Despite this widely recognised role of leaf‐cutting ants as key herbivores of neotropical ecosystems, there is only limited knowledge available about the fitness consequences of their harvesting activities at the single plant level (but see Câmara et al, 2019; Farji‐Brener & Tadey, 2017; Mundim et al, 2012). These few available studies on the effects of leaf‐cutting ant herbivory on plant reproduction report contrasting results with negative impacts on flower production (Câmara et al, 2019; Mundim et al, 2012), but also no effects on fruit set (Câmara et al, 2019; Farji‐Brener & Tadey, 2017). Interestingly, the absence of such effects may be related to the plants' limited recognition of leaf‐cutting ant herbivory.…”

“…we randomly selected five branches to track the evolution of preanthesis floral buds monthly from February to April 2020. To evaluate the reproductive success of the plants, we adopted the reproductive success metrics byCâmara et al (2019): (1) 'floral bud production' as the number of floral buds, (2) 'flower production' as the number of flowers, (3) 'fruit production' as the number of fruits and (4) 'fruit set' as the proportion of buds + flowers that turned into fruit. To calculate the fruit set, we summed the number of floral buds and flowers observed during the first and second observations and divided that by the number of fruits counted in the third and final observation at the end of the reproductive cycle.…”