Time will tell: Larger and less abundant fruit-feeding butterflies (Lepidoptera: Nymphalidae) are synchronized with food availability in the Brazilian Cerrado

doi:10.21203/rs.3.rs-1602292/v1

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Research Article

Time will tell: Larger and less abundant fruit-feeding butterflies (Lepidoptera: Nymphalidae) are synchronized with food availability in the Brazilian Cerrado

https://doi.org/10.21203/rs.3.rs-1602292/v1

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published 03 Jun, 2023

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Introduction: Diet and temporal specialists, especially those in tropical seasonal environments, require synchronous phenology with hosts. Species with life-history-traits that covary with temporal specialization may be particularly vulnerable to climate-driven changes in phenology. In the Cerrado, larger fruit-feeding butterflies species tend to be less abundant and more seasonal than their smaller-bodied relatives. It is important to consider how ecological process and phylogenetic history are associated with these attributes.

Aim/Methods: Here we evaluated the effects of climate and body size on the seasonality of abundance of fruit-feeding butterflies as well as their association with natural history traits including diet breadth and synchrony with fruits.

Results: The distribution of abundances of these butterflies species was not uniform throughout the year, was associated with body size and shaped by habitat type and climate. Overall, hot and wet months were associated with higher abundance and species richness of these nymphalids in the Cerrado. Lineages of large-bodied species were less abundant, more seasonal and more generalized in larval diet breadth. In addition, these large-bodied clades were more tightly synchronized with fruit phenology.

Discussion: Our findings support the hypothesis that large and less abundant species to occur in a narrow temporal window and synchronized with fruit phenology.

Implications for insect conservation: Particular attention should be given for the conservation of larger-bodied temporal specialist species as they are vulnerable to phenology mismatching as a result of rapid global warming, but they will also face additional pressures with the advancing deforestation in the Cerrado.

Body size

Cerrado

Climate Change

Evolutionary History

Herbivory

Nymphalids

Climate Driven phenological changes pose substantial ecological consequences (Parmesan 2006), with implications for individual fitness, population persistence, species conservation, and community structure (Miller-Rushing et. al. 2010, Diamond et al. 2011; Hill et al. 2021). Responses ar far from uniform (Macgragor et al. 2019), and can vary in magnitude and direction even in species experiencing similar environmental conditions (Macgragor et al. 2019; Hill et al. 2021). Due to their extreme diet specialization, plan-herbivore interactions are particularly vulnerable to climate-driven phenological and ontogenetic changes. Phenological decoupling with hosts (Stireman et al. 2005; Memmott et al. 2007), and ontogenetic effects, such as those mediated by changes in body size, that limit dispersal and fecundity, are factors that can limit viable population sizes if these interactions are not realized in space and time.

Insects, including butterflies, have been proposed as informative organisms for testing climate impacts on ecological communities, because they show rapid responses to changes in the environment given their short generation times and their particular ecological requirements (Hill et al. 2021). Despite the bulk of evidence showing that insects are rapidly disappearing rapidly due to climate change (Stireman et al. 2005; Diamond et al. 2011; Hill et al. 2021), there is still a need for more studies to investigate which life history traits co-vary with temporal-related traits, in order to enable us to make better predictions about species response in the face of environmental change (Pavoine et al. 2014; Spaniol et. al. 2019). This is particularly relevant for species inhabiting environments with a marked seasonality, such as the Brazilian Cerrado (Stevens et al. 2012; Fountain-Jones et al. 2015).

The Cerrado is the second largest biome in South America and the most biodiverse savannah in the world (Silva & Bates 2002; Klink & Machado 2005). It covers a wide latitudinal and environmental gradient and is composed of a mosaic of plant formations from open grasslands (7%) to dense forests (32%), while most of its area (61%) is typically woodland savannah (Marquis et al. 2002). The Cerrado has well-defined dry and rainy seasons, with an average rainfall around 1,400 to 1,500 mm per year, which is 80% distributed between October to March (Silva et al. 2008). The dry season (May to September) is severe and impose important constraints on the persistence of animal communities (Marquis et al. 2002). Seasonal changes in temperature and water availability from the dry to the wet season, triggers primary production promoting intense leaf production and greater availability of ripe fruits, which are essential for immature and adult butterflies, respectively (Morellato et al. 2000; Ribeiro et al. 2010). In addition, the water availability may directly affect the occurrence of these butterflies (Brito, et al. 2021). This, it is especially important to understand the relationship between weather conditions and butterfly survival as Cerrado high deforestation rate is leading to a change in climate, which is generally becoming hotter and drier (Hoffman et al. 2021). These changes can have severe consequences for the survival and persistence of different butterfly species inhabiting the landscape, since some species can be negatively affected by dry conditions (Freire-Jr et al. 2014).

Rainfall is the main predictor of insect emergence in the Tropics, with the onset and cessation of rains playing an important role in the regulation of insect activity pulse (Wolda 1988). Consequently, air temperature and humidity are generally positively associated with the abundance and species richness of insect communities, with examples from ant (Dáttilo & Vasconcelos, 2019) and butterfly species (Brown Jr. 1992; Ribeiro et al. 2010; Freire-Jr & Diniz 2015; Lourenço et al. 2019). However, this relationship might be more complex than previously understood. Although seasonality explains the temporal dynamics of fruit-feeding butterflies (nymphalids) in the Cerrado, subfamilies with varying body sizes differ in their temporal distribution (Ribeiro & Freitas 2011; Freire Jr. & Diniz 2015), indicating that body size therefore may contribute to the temporal dynamics of these butterflies.

The yearly temporal distribution of small-bodied fruit-feeding butterflies tends to be longer than their larger relatives (Ribeiro & Freitas 2011). One possible explanation is that the higher energetic demand of larger species constrains them to occur in a narrow time period when optimal resources are available (Brown et al. 2004; Ribeiro & Freitas 2011). Moreover, small-bodied species tend to have shorter lifespans, despite their wider temporal distribution, greater abundances, and narrower larval diet breadths (Hjalmarsson et al. 2015; Freire-Jr. et al. 2021.a; Sudta et al. 2022). Although the association between diet breadth and temporal distribution is poorly understood in butterflies, our expectation is that the temporal distribution of smaller and more specialized butterfly species will be less restricted throughout the year compared to their larger relatives (Pozo et al. 2008; Ribeiro & Freitas 2011; Freire Jr. & Diniz 2015).

Nonetheless, trait-environmental relationships may not be exclusively explained by present-day ecological processes but can also reflect the evolutionary history shared by species in ecological communities (Pavoine et al. 2014; Duarte et al. 2018). Thus, phylogenetic information, especially when combined with both ecological and functional methods, is essential for a more accurate understanding about community assembly (Spaniol et al. 2019). However, the strength of phylogenetic signal remains underused in studies attempting to uncover the influence of body size on temporal dynamics (Ribeiro & Freitas 2011; Spaniol et al. 2019; Freire-Jr et al. 2021a) for most insect populations, particularly in the Cerrado, where temporal dynamics are an important part of the ecological dynamics that influence different animal species (Silva et al., 2011; Freire Jr. & Diniz, 2015).

Fruit-feeding butterflies (Nymphalidae) use rotting fruit as an important food resource. They comprise about 50-75% of all Neotropical species richness in this family (DeVries et al. 1999; Brown Jr., 2005), are easily sampled with a standardized trap protocol (Uehara-Prado et al. 2007; Freitas et al. 2014), and respond consistently to environmental changes in space and time (Ribeiro et al. 2010; DeVries et al. 2016). Therefore, fruit-feeding butterflies are frequently used as models in environmental studies and biodiversity monitoring plans (see GEOBON, GBIF).

Here we evaluated factors that influence the temporal patterns of abundance (hereafter, seasonality of abundance) of fruit-feeding butterflies as well as other natural history traits while considering their evolutionary histories, and addressing two ecological questions:

1) What are the seasonal patterns of abundance and richness and how do these patterns vary with climate and habitat? We expect a positive influence of temperature and humidity on both species abundance and richness of these butterflies (Ribeiro et al. 2010; Lourenço et al. 2019), which is tightly associated with the phenology of adult food resources (ripe fruit) in the Cerrado (Batalha & Mantovani 2000; Guarino & Walter 2005; Silva–Jr. & Sarmento 2009).

2) Among butterflies in the Cerrado, is the seasonality of abundance, diet breadth and host plant synchrony associated with important life history traits such as body size? Since body size is strongly related to species metabolism, we expect larger butterflies to occur in a narrower temporal window compared to their smaller relatives. Moreover, since body size and diet breadth are phylogenetically conserved (Spaniol et al. 2019, Freire-Jr. et al. 2021.a), we expect an indirect effect of phylogeny on the temporal distribution of these butterflies. Therefore, we expect the occurrence of larger, more generalist, and more seasonal butterflies to be more synchronized with the optimum food resources period than their smaller relatives.

Study site and Sampling methods

This study was performed from July 2012 to June 2013 in Fazenda Água Limpa (FAL), which covers an area of 4,500-ha (15º56`23``S e 47º56`26``W), Brasília, Federal District, Brazil (Figure 1). The study site is inside a 10,000-ha protected area (Fonseca and Silva–Jr. 2004). We established five linear transects (200 m) 1 km apart from each other in two habitats: savannah woodland and gallery forest. In each of these two habitats, we distributed 15 plots (3 plots per transect), containing two bait traps stratified at different heights: canopy (~8 m) and understory (~ 1.5 m) for a total of 60 bait-traps. Following an established protocol (DeVries et al. 1999; Freitas et al. 2014), traps were baited with a mixture of sugarcane and bananas (~50 mL) fermented for 48 h to attract fruit-feeding-only nymphalids were sampled. Samples were collected for five consecutive days during the first week of each month. Traps in both habitats were visited and had their bait replaced every 48 h. Samples captured in the canopy and understory were combined to calculate species richness and abundance per plot. Two specimens from each species were collected and deposited as vouchers at the Entomological Collection of the Zoology Department of the University de Brasilia (UnB), Brasilia, Brazil.

Seasonality of Nymphalid abundance

We applied circular statistics to evaluate the temporal patterns of abundance distributions for each subfamily or tribe, hereafter referred as “clade”. With consideration to its periodic nature and the clustering of events, circular statistics is a more intuitive approach for phenological data (Staggemeier et al.2019). This approach involves the transformation of data in linear or ordinal scales to a circular scale (angles or radians) and then converted to cartesian coordinates. Various descriptive statistics can be computed using trigonometric functions on the vectored data (Cremers & Klugkist 2018). We focused on the mean vector length (r) which is one of the more informative metrics for phenological data since it can be interpreted as the degree of seasonality. The mean vector length summarizes the spread of vectored data along the circular distribution which, in the study, measures the extend of clustered species abonances throughout the year. Values for r range from zero (low clustering-record are randomly oriented) to one (complete clustering-all records occurred in the same sampling period) (Zar 2014). The significance of mean vector length was assessed using the Rayleigh test. This significance test evaluates the null hypothesis assuming uniformly distributed data (assumes an underlying Von Rises distribution) against the alternative hypothesis which implies data cluster and are not uniformly distributed. This analysis was performed with the package “circular" (Agostinelli & Lund 2017) in R (R Core Team 2020). The circular distributeions and their mean vector length for each clade are illustrated using rose plots. Species with less than six individuals were removed from the analysis (Landler et al. 2020).

Body Size

We photographed ten specimens of each species to quantify forewing length (FWL) using ImageJ (Schneider et al. 2012). We considered FWL a surrogate for body size, as the correlation between wingspan and body length is about 0.8 in fruit-feeding butterflies (Shahabuddin & Ponte 2005).

Larval Diet-Breadth

We reviewed literature to create a matrix of host plant-herbivores associations for sampled taxa (Beccaloni et al. 2008). To reduce bias from incomplete host records, the host plant matrix was reviewed and edited using expert knowledge from Dr. André V.L Freitas. The edited matrix was used to calculate the taxonomic diet breadth,the known number of host plant families, genera, and species consumed by larvae of each butterfly species, and the phylogenetic diet breadth. To estimate phylogenetic species-level diet breadth, we used phylogenetic diversity (Faith 1992) among host plant species in the R package picante (Kembel et al. 2020). We applied the most recent angiosperm phylogeny (Zane et al. 2014) using the V.PhyloMaker package (Jin & Qian 2019).

Nymphalidae Phylogeny

Phylogenetic relationships were estimated at the species using the phylogeny published in Wahlberg et al. 2009. This phylogeny was inferred based on 10 genes and 250 morphological characters for 400 valid genera from Nymphalidae (Wahlberg et al. 2009). Missing species branches were pruned from the original phylogeny. To include species that were absent from the published phylogeny, we reviewed topologies from the specific taxonomic literature and consulted with experts. Branch lengths of the imputed species were determined as half of the branch lengths from the same node on the original tree (Supplementary Material)

Species temporal distribution, body size and diet breadth

The temporal distribution of species abundance was tested using circular statistics. This approach allows testing how concentrated are species abundances throughout the year using the “mean vector length (r)". The (r) values range from zero (random orientation) to one (if all records occurred in the same sampling period) (Zar, 2014). The significance of mean length was assessed using the Rayleigh test, which assumes a unimodal distribution as an alternative hypothesis. This analysis was performed with the package “circular” (Agostinelli & Lund 2017) in R (R Core Team 2020). Species with less than six individuals were removed from the analysis (Landler et al. 2020).

Synchrony with Plant Phenology

A plant inventory for both woody plants (DBH ≥ 5cm) and herbaceous/shrubs (DBH ≤ 4cm) was performed in each of 30 plots (100m²) where bait-traps were installed. We determined the period of fruit ripening for inventoried plant species using published literature about plant phenology in the Cerrado (Batalha & Mantovani 2000; Guarino & Walter 2005; Silva-Jr. & Sarmento 2009). Among this subset of fruiting plants, the number of plants that presented mature zoochorical fruits were counted each month.

Synchrony was defined as the pseudo-R statistic from a generalized linear model with a Poisson link function regressing relative butterfly abundance against the associated number of plant species with mature fruits in a given month. A model was made for each butterfly clade.

Climate variables

The monthly (Jul/2012 to Jun/2013) data of air temperature (max. ºC) and air humidity (min. %) were obtained from RECOR's Climatic Station (online at: http://www.inmet.gov.br), which is 2 km from the study site (hereafter defined as macroclimate). Additionally, six dataloggers (HOBO U23-001), programmed to record air temperature (max. and standard deviation – sd.) and air humidity (min. and sd.) every 15 minutes were equally distributed in both savannah woodlandand gallery forest (hereafter defined as microclimate). Measurements were done monthly during the same week in which butterflies were sampled.

Generalized Linear Models

We built two generalized linear models with Poisson distribution to test the effect of air temperature (max. and sd.) and humidity (min. and sd.) and habitat (savannah woodland and gallery forest) on the monthly species abundance and richness, respectively. In addition, the interaction between microclimate and habitat was investigated. All climate predictors were included in the first model (full model). Later, we excluded variables with lower predictive power. Model fit was evaluated using Akaike Information Criterion (AIC values) (Logan, 2010). Extreme outliers were identified using residuals vs. leverage plots.

Phylogenetic generalized least squared models

We calculated Blomberg's K statistic to estimate phylogenetic signal for body size, abundance, diet breadth, and seasonality of abundance (Blomberg et al. 2003). To control for non-independence due to the phylogenetic history of the taxa investigated we applied phylogenetic generalized least square models (PGLS). The models estimated the linear relationships between body size and the following response variables: abundance, seasonality of abundances, diet breadth, synchrony with food resources period (Blomberg et al. 2003). This method incorporates information about relatedness into the error term, assuming a model of trait evolution (Brownian model) (Symonds & Blomberg 2014). The PGLS models were built considering both species and clades independently. All analyses were performed using the R software packages ape, picante, payrolls (Paradis, & Schliep 2019; Kembel et al. 2020; Reve 2012).

Nymphalidae seasonal abundance

We sampled 3,321 individuals from 30 nymphalid species (Supplementary data S1). The abundance distribution of nymphalid clades was not uniform throughout the year (Figure 2). The abundance peaks of Satyrini, Brassolini, Biblidinae, and Nymphalinae, occurred between March – April, Morphini in November, and Charaxinae in June (Figure 2a-f, Appendix S1). The highest mean vector length occurred in Morphini (r = 0.27, Figure 2e), followed by Nymphalinae (r = 0.24, Figure 2c), and Brassolini (r = 0.21, Figure 2f). Charaxinae (r = 0.16, Figure 2d) and Satyrini (r = 0.11, Figure 2a) were those with lower mean vector length.

Effects of climate and habitat on the temporal patterns of abundance and richness

Abundance (Figure 3a) and species richness (Figure 3b) were positively associated with air humidity and temperature, explaining 40% and 30% monthly variation in these variables, respectively (Table 1). Morphini (Figure 4a) was positively influenced by air temperature (beta = - 0.37; R²: 0.2; P = 0.004), and Satyrini (Figure 4b) was positively influenced by air humidity (beta = 0.23; R²: 0.59; P = 0.013), which explained 20% and 59% of the temporal abundance distribution of each clade, respectively.

Table 1. Results of generalized linear models with Poisson distribution testing the effects of macroclimate variables against a) abundance, b) nymphalid species richness captured from July/2012 to June/2013 at Fazenda Água Limpa, Brasília, Brazil.

Response var./ Factors		α/β	d.f_num	d.f_den	Dev	Res dev.	t	F	P
a) Abundance
Intercept	-1.1		-	10	-	1062.1	-0.38	-	-
Air temp. max(ºC)	0.18		1	9	98.3	963.7	2.13	1.4	0.2
Air humid. min (%)	0.02		1	8	421.6	542.1	2.41	6.06	0.03

b) Species richness
Intercept	1.65		-	10	-	13.6	2.02	-	-
Air temp. max(ºC)	0.05		1	9	4.02	9.5	2.02	4.02	0.04

Lower variation in temperature was associated with higher butterfly abundance (beta = - 0.99; P < 0.001) and species richness (beta = - 0.07; P ≤ 0.04), in both the gallery forest and savannah woodland (Table 2). Humidity was positively associated with species richness in both savannah and gallery forest (Table 2). Moreover, higher species abundance was observed when air humidity was unstable in savannah woodland (Table 2).

Association of body size with seasonality of abundance, diet breadth and host plant synchrony

Body size (K = 1.18; P = 0.001), larval taxonomic diet breadth (K = 0.6; P = 0.02), and phylogenetic diet breadth (K = 1.01; P = 0.003) exhibited phylogenetic signals (Figure 5a). Although some smaller species were highly abundant, body size was not an important predictor of abundance at the species level (beta = -0.18, pseudo-R²: 0.05; P = 0.59; Figure 5b). Conversely, body size was negatively associated with abundances of different clades (beta = -0.82, pseudo-R²: 0.7; P = 0.03, Figure 5c). Satyrini (FWL = 22 mm; N = 1,657 – 48%) and Biblidinae (FWL = 27 mm; N = 1,391 – 40%) were the clades composed by smaller and relatively abundant species, followed by Charaxinae with intermediate body sizes (FWL = 28 mm) and abundances (N = 192 – 6%), compared to the larger and less abundant Brassolini (FWL = 52 mm; N = 30 ind. – 0.9%) and Morphini (FWL = 59 mm.; N = 10 ind. – 0.3%) (Figure 5c).

Table 2. Results of generalized linear models testing the association between microclimate (maximum air temperature–ºC and minimum air humidity–%), abundance, and nymphalid species richness captured in three plots in Savannah woodland (S1 – S3) and three points in the gallery forest (F1 – F3) from July/2012 to June/2013 at Fazenda Água Limpa, Brasília, Brazil. (*) represents p ≤ 0.05; (**) p ≤ 0.01; (***) p ≤ 0.001.

Response var./ Factors	α/β	d.f_num	d.f_den	Dev	Res dev.	F	P
Abundance
Intercept	-6.59	-	23	-	1875.6	-	-
Habitat	-1.53	1	22	417.4	1458.1	14.97	**
Air temperature - SD.	-0.99	1	21	536.3	921.7	19.24	***
Air humidity - SD.	0.17	1	20	129.1	792.6	4.63	*
Air humidity - SD.: Habitat	-0.19	1	19	251.9	540.7	9.03	**
Species richness
Intercept	0.97	-	23	-	1.41	-	-
Habitat	0.05	1	22	0.83	0.57	45.1	***
Air humidity - mean	0.001	1	21	0.12	0.44	6.8	**
Air temperature - SD.	-0.07	1	20	0.08	0.36	4.3	*

Association of body size with seasonality of abundance, diet breadth and host plant synchrony

Body size was a weak predictor of seasonality at the species level (beta = -0.05; P = 0.31; Figure 5d) but it explained about 62% of the variation on seasonality of each clade (beta = + 0.55; P: 0.018; Figure 5e), in which large-bodied clades were more seasonal than their smaller relatives. In addition, body size was positively associated with both phylogenetic diet breadth (beta = 0.03; pseudo-R²= 49%; P < 0.03; Figure 5f) and synchrony with fruits (beta = 1.92; pseudo-R²= 55%; P < 0.01). Larger-bodied clades were more generalized in their larval diet breadth, and tightly associated to the peak of ripe fruit availability compared to their smaller relatives (Figure 5g).

Satyrini (pseudo-R²: 0.04) and Charaxinae (pseudo-R²: 0.13) were weakly synchronized with the peak occurrence of fruits; whereas Nymphalinae (pseudo-R²: 0.22) and Biblidinae (pseudo-R²: 0.28) were moderately synchronized. Both Brassolini (pseudo-R²: 0.32), and Morphini (pseudo-R²: 0.83) were tightly synchronized with the peak occurrence of fruits. However, these associations were only significant to Morphini (beta: + 0.21; pseudo-R²= 83%; P < 0.001).

This is the first report of the associations between body size, diet breadth and seasonality for fruit-feeding butterflies in the Cerrado. Results reinforce the bimodal pattern on temporal abundance distributions of these nymphalids in the Cerrado, mainly associated with hot and wet months (Freire-Jr. & Diniz 2015). This finding highlights the importance of considering both transitions dry-wet and wet-dry in short-term studies to optimize the sampling effort for fruit-feeding butterfly guild in Cerrado (Freire-Jr & Diniz 2015). In addition, phylogenetic signal was found for both body size and diet breadth, indicating trait conservatism, where close relatives have similar body sizes (Duarte et al. 2014; Graça et al. 2017; Spaniol et al. 2019) and similar host-plant associations (Freire-Jr. et al. 2021a). This reiterates the importance of considering clade evolutionary history when examining their complex trait–environment relationships.

The higher species abundance and richness associated with hot and wet months is recurrently reported for insects (Kishimoto-Yamada & Itioka 2015), including butterflies in other tropical region sites (DeVries et al. 1999; Ribeiro et al. 2010, 2016; Brito et al. 2014; Grøtan et al. 2014; Lourenço et al. 2019). It has been frequently proposed that butterfly life cycles are synchronized with periods of optimum abiotic conditions (Ribeiro et al. 2010; Silva et al. 2011; Lourenço et al. 2019), resource availability, and low enemy pressures, collectively known as “temporal window” (Brown-Jr. 1992; Morais et al. 1999; Ribeiro & Freitas 2011).

Temperature is a key factor in accelerating developmental rates and adult reproductive activity in insects (Wolda 1988). Additionally, higher temperatures and water availability, triggers primary production that promotes intense leaf production and greater availability of ripe fruits, which are both essential resources for immature and adult butterflies, respectively (Morellato et al. 2000; Fischer et al. 2004), potentially explaining the temporal dynamics of these butterflies.

A pronounced and positive effect of humidity on nymphalid abundance and species richness was observed, which lead all clades but Charaxinae to occur preferentially during the rainy season. This is highly concerning as it suggests that most butterfly species might be affected by changes in Cerrado climate due to deforestation, where different parts of Cerrado's area are becoming drier (Hoffman et al. 2021). The only exception was Charaxinae, which is well known to inhabit forest canopies and open habitats where the microclimate is hot and dry (Lourenço et al. 2019; Freire-Jr. et al. 2021b). Thus, climate change could result in the expansion of their current ranges and increase their adaptability to future microhabitats created by these shifts.

Nevertheless, the temporal dynamics for all other clades reinforce the hypothesis that the severe dry season of the Cerrado may impose harsh conditions on animal communities (Marquis et al. 2002; Silva et al. 2008). It is especially concerning when considering small-bodied butterflies, which are particularly vulnerable to desiccation (Fischer & Kirste 2017; Brito et al. 2021). Thus, particular attention should be given for the conservation of smaller species as they are more vulnerable to current changes in climate, but will also face additional pressures with the advancing deforestation in the Cerrado.

The negative association between body size and abundance at the clade level indicates that large-bodied taxa were less abundant than their smaller relatives, reinforcing patterns observed in other animal taxa, including mammals, beetles, moths and butterflies (Damuth 1981; Morse et al. 1985; Gillespie et al. 2016; Zhang et al. 2019; Sudta et al. 2022 Freire-Jr et al. 2021a). It can be a consequence of the energetic trade-off between body size, abundance and temporal specialization (White et al. 2007), which forces the larger and less abundant butterflies to occur in a narrow “temporal window”, when optimum conditions of climate, food resource, and low enemy pressures are available (Morais et al. 1999; Ribeiro & Freitas 2011; Gillespie et al. 2016). In fact, we have found that large and less abundant fruit-feeding butterfly clades, such as Morphini and Brassolini, were more temporally restricted in their distribution (greater circular - r) and highly synchronized with fleshy fruit occurrence than their smaller relatives.

Additionally, our results suggest a potential tradeoff between temporal specialization and dietary specialization of fruit feeding butterflies in the Cerrado, resulting in the observed patterns of seasonal abundance. A wider diet breadth may enhance the fitness of those large-bodied but temporally restricted butterflies. In addition, it may provide a higher variety of host plants for adult oviposition, and consequently for feeding their caterpillar development and growth. Moreover, phenology mismatching as a result of rapid global warming (Stireman et al. 2005; Diamond et al. 2011; Hill et. al. 2021; Wolkovich & Donahue 2021) may impose a greater risk to larger-bodied butterflies that are potentially more synchronized with fruit phenology.

AKNOWLEDGMENTS

The authors would like to thank Fernando Carvalho, Miguel Marinho, and Nayara F. Araújo for their assistance with fieldwork. Thanks to the University of Brasília for the logistical support. G.B.F.Jr and I.R.D are grateful for the financial support provided by the Coordination of Improvement of Higher Education (CAPES) and the National Council for Scientific and Technological Development (CNPq) through the PVE Program and PRONEX CNPq/FAPDF (research fellowship grant: CNPq-303076/2013), respectively. Special thanks to André Lucci Freitas, Lee Dyer, Pedro Constantino, Celso Oliveira, Korynna Rubio, and Andrea Glassmire for their important contributions to specimen identification and comments on a previous version of this paper.

CONFLICT OF INTEREST

The authors declare no conflict of interest.

DATA AVAILABILITY

The data that support the findings of this study are available in the supplementary material of this article.

AUTHOR CONTRIBUTION

G.B Freire-Jr, I.R. Diniz, conceived, designed the experiment and have edited the manuscript. T. Silva, J.P. Dias, and H.P. Rodrigues performed the fieldwork, J.P.Santos, built the phylogenetic tree; D.B. Ribeiro, and D. Provete analyzed the statistical analyses. G.B.FJr, D.M. Salcido, and H.FM. Oliveira, wrote the manuscript.

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Time will tell: Larger and less abundant fruit-feeding butterflies (Lepidoptera: Nymphalidae) are synchronized with food availability in the Brazilian Cerrado

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