The role of frugivores in the formation of novel
interactions
A comparative study of avian frugivore traits shaping novel palm-bird
interactions in the Atlantic Forest
Kirian Schreuders
BSc Project
Daniel W. Kissling
Caroline Darcxler
July 10, 2020
Abstract
Introduction of an animal-dispersed plant species into a new environment often leads to the formation of novel interactions with frugivores in the ecological community present. Assessment of frugivore traits is crucial to understand mechanisms shaping plant-frugivore interactions and plant invasion. The aim of this study was to understand how frugivore traits contribute to the formation of novel plant-frugivore interactions. A comparative trait analysis was performed to understand how plant-frugivore trait values differed between two groups of birds; 1) bird species interacting exclusively with native palm species and 2) bird species interacting with both native and alien palm species in the Atlantic Forest, Brazil. Data on palm-bird interactions was merged with bird trait data to asses group differences for the traits body mass, extent of occurrence and degree of frugivory. Results showed that body mass was similar for both groups which indicates compatibleness of the introduced palm species with the ecological community in the Atlantic Forest. Furthermore, novel palm-bird interactions in the Atlantic Forest are shaped by birds that co-occur with many plant species, but are not necessarily highly fruit dependent. With the use of a new comprehensive interaction dataset, this study showed that comparative trait analysis of frugivore traits can be performed to determine how they shape the formation of novel plant-frugivore interactions.
Acknowledgements
The completion of this BSc project would not have been possible without the help and guidance of numerous people. First of all, I would like to thank my supervisors Caroline Dracxler and Daniel Kissling for brainstorming about subjects, putting me on the right track and providing feedback on earlier versions of this project and report. Caroline, thank you for letting me lend and use a part of your current life’s project, the interaction dataset, and for your intensive support and guidance. It was always nice to see you smiling behind the camera in Brazil. Even though times were sometimes though, for me the Skype meetings twice a week were a time to laugh, put things in perspective and reflect on the ongoing process. Daniel, thank you for taking your time and guiding me in doing a project on my interests. Secondly, I would like to thank all my fellow students, Beta-Gamma and Biology, for the great years in- and outside the university. The life lasting friendships resulting from that first year of Beta-Gamma are most precious to me. Thank you colleague biologists for the fun and outgoing fieldtrips we made where I not only learned about the practical side of biology, but also about the in situ conditions of the biologist itself. Lastly, I would like to thank my friends and family. Thank you Benjamin, Bouke and Levi for not only being amazing fellow BG’s, but also for being amazing friends, supporting me when things were not as bright, laughing, reflecting and being an inspiration to this project and my life the past four years. Bram, thank you for your peer review and for your ‘long-distance’ and true friendship. Pap, mam and Igor, thank for your support during the difficult times in which I was working on this project. Even though things have not been easy at all times, I feel the sometimes life-changing experiences we had to endure encouraged us all to be more authentic, loving and open towards ourselves and each other. Pap, thank you in specific for the shelter in Tiel where I was able to ground and keep going to finish this project that I can be proud of.
Contents Abstract ...2 Acknowledgements ...3 Introduction ...5 Methods ...7 Results ...8 Discussion... 10 References... 13
Introduction
Arrival of an alien plant species into a new environment – often by human cultivation or trade - can result in the formation of novel interactions of the species with the ecological community present (Traveset & Richardson, 2014). These interactions can be antagonistic when plant seeds are predated or mutualistic when seed dispersal of a fruiting plant is facilitated by fruit-eating animals, also known as frugivores. Success of animal-dispersed alien plants depends on the formation of the latter interaction; seed dispersal must be facilitated by the ecological community in order for the plant to spread away and form new populations (Richardson et al., 2000). Because of their often generalized diet and high abundance especially in tropical systems, frugivores are responsible for the dispersal of many native and alien plant species (Jose et al., 2013). Subsequently, many ecological communities in tropical environments are often readily able to form novel interactions with introduced plant species (Traveset & Richardson, 2014).
The formation of novel interactions between alien fruiting plants and frugivores depends on plant and frugivore traits (Buckley et al., 2006). Whether an alien plant can compete with native plants in attracting frugivores for seed dispersal depends on the trait diversity of the alien plant (e.g. plant height, fruit colour and conspicuousness, fruit texture) (Ordonez et al., 2010; Mengardo & Pivello, 2012). Moreover, frugivore traits and compatibleness between plant and frugivore traits are crucial to determine if novel interactions can exist (Bender et al., 2018; Buckley et al., 2006; Gosper et al., 2005). Frugivore diet specialization and generalization can indicate the likelihood that a frugivore species will form novel mutualistic interactions with fruit-carrying alien plants. Generalist frugivores, as opposed to more specialist species, are known to play an key role in dispersing many native and alien plant and therefore shaping plant-frugivore networks (Jordaan et al., 2011; Palacio et al., 2016). Functional frugivore traits, such as degree of frugivory, can be used to assess the importance of fruit-dependency in the formation of novel interactions. Furthermore, compatibleness between frugivores and alien plants is determined by morphological frugivore traits such as body mass (e.g. a large body mass allows for eating large or many fruits) and wing-shape in birds (Bender et al., 2018; Schupp et al., 2010).
Plant-frugivore interactions and the role of native and alien plant traits have been studied extensively to assess the importance of these interactions and plant traits in plant invasions (Bender et al., 2018; Deckers et al., 2008; Hulme & Bernard-Verdier, 2018; Ordonez et al., 2010). Knowledge on frugivores and their traits provides a key component in understanding contributing factors shaping interactions and plant invasions (Buckley et al., 2006), but in contrast to assessments of plants traits, comparative studies of frugivores interacting with native and alien plant species are still missing. Conducting a comparative analysis of frugivore traits will generate new knowledge on the contribution of frugivore traits in the formation of novel interactions between alien plants and frugivores. Hence,
this study focusses on the difference in frugivore traits between two groups of frugivores; (1) avian frugivore species that exclusively interact with native palm species and (2) avian frugivore species that interact with both native and alien palm species in the Atlantic Forest in Brazil. An interaction is counted as a frugivore species feeding on palm fruits or predating its seeds.
Avian frugivores make a good model group to study because they are known to be the biggest disperser group of alien fruiting plants (Jose et al., 2013), and interaction and trait data is abundantly available (Bender et al., 2018; Wilman et al., 2014; Dracxler, unpublished). Palms (Arecaceae) are a key fruit resource for tropical birds and often dependent on frugivores for seed dispersal, which makes them a good model group for studying the formation of novel interactions between plants and frugivores (Galetti & Aleixo, 1998.; Galetti, 1996, as cited in Genini et al., 2009). In addition, tropical palms are often cultivated as ornamental plants outside of their native range which makes them likely to invade new ecological communities, as has happened with Archontophoenix cunnighamiana (Mengardo & Pivello, 2012) and Livistona chinensis (Foxcroft et al., 2008). The Atlantic Forest is a Neotropical forest and biodiversity hotspot that stretches along the coast of northeast Brazil towards the south of Brazil and the north of Paraguay and Argentina (The Nature Conservancy, 2020). Because of its unique and high biodiversity, the ecology of the forest has been studied extensively (Genini et al., 2009; Petri et al., 2018; Rezende et al., 2018) and plant-frugivore interaction records are abundant (Bello et al., 2017; Dracxler, unpublished), making the Atlantic Forest a good study site for a comparative study of frugivore traits.
The following traits will be assessed for the frugivore groups: body mass, extent of occurrence and degree of frugivory. Compatibleness of the ecological community with alien palm species will be assessed using frugivore body mass. The contribution of diet generalization and dependency in the formation of novel interactions will be investigated using extent of occurrence – the total area of a species’ occurrence - and degree of frugivory, the percentage of fruits and seeds in the total diet. For each trait a hypothesis is formulated. (1) Body mass is expected to be similar for both frugivore groups, because a successful palm invasion requires compatibleness of the alien palm with the total assemblage of frugivore species and this can be reflected in similar body mass values. (2) Extent of occurrence is expected to be larger for frugivore group 2, because frugivore species with a large extent of occurrence will co-occur with a high number plant species and might therefore constitute a large part of the frugivore species interacting with alien plant species. (3) Degree of frugivory is expected to be higher for frugivore group 2, since frugivore species highly dependent on fruits are more likely to include alien fruit into their diet (Debussche & Isenmann, 1990; Gosper et al., 2005).
Methods
Data on palm-bird interactions were used to identify frugivore species that exclusively interact with native palm species and frugivore species that interact with both native and alien palm species. The interaction data used is a subset of a dataset on palm-frugivore interactions in the Neotropics collected in literature (Dracxler, unpublished). The subset used in this research is compiled of 791 palm-bird interactions recorded in the Atlantic Forest, including the following botanical countries: Brazil Northeast (BZE), Brazil Southeast (BZL) and Brazil South (BZN).
Interactions were sorted into three frugivore groups and deduplicated to make sure only unique interactions remained. Group one consisted of frugivore species exclusively interacting with palm species native to the Atlantic Forest. Group two consisted of frugivore species that interact with palm species that are native and alien to the Atlantic Forest. Group three was compiled of frugivore species that only interact with alien palm species.Due to small sample size of group three (N = 5), only group one and two (N = 52 and N = 32, respectively) were included in final statistical analysis.
Trait values were compiled using Elton Traits 1.0, a dataset on morphological and functional bird traits that play a key role in species’ ecosystem functioning (Elton Traits 1.0 ; Wilman et al., 2014). From Elton Traits 1.0 species’ values for body mass (in grams) (Smith et al., 2003 & Dunning, 2007, as in Wilman et al., 2014) and the proportion of diet items in the total diet were extracted. Trait values were then merged to the unique interactions using the R package dplyr (Wickham et al., 2020). The degree of frugivory was calculated from the proportion of diet items as the percentage of fruits plus seeds in the total diet of frugivore species. Extent of occurrence (in km2) was extracted manually for each frugivore species from IUCN Redlist data on estimated extent of occurrence (IUCN, 2020).
After merging and completion of trait values for each frugivore species, statistical testing was performed to test differences in trait values for frugivore groups one and two. For every trait, univariate analysis was performed with the trait as the dependent and the frugivore groups as the independent variables. A Shapiro-Wilk test for normality and a Levene’s test for equal variances were performed using R package car (Fox & Weisberg, 2019) to determine the most accurate type of statistical test needed. Subsequently a non-parametric Mann-Whitney U test was executed to test differences for the two independent frugivore groups. Data was managed and visualized using R package reshape2 (Wickham, 2007) and ggplot2 (Wickham, 2016). All data handling and statistical testing was executed in R version 3.6.3 (R Core Team, 2020) and use was made of packages that are part of R unless mentioned otherwise.
Results
A total of 87 unique bird species was found interacting with 11 palm species, 8 of which are native and 3 of which are alien to the Atlantic Forest. From the bird species, 55 interact with native palm species and 32 interact with both native and alien palm species (table 1). Clearly visible is that the number of bird and palm species was different for both frugivore groups. The larger sample size and higher number of palm species in frugivore group 1 indicated more unique interactions and thus more robust results for this group.
Frugivore group
Number of frugivore
species Palm species
Median body mass (g) ± MAD Median extent of occurrence (km2) ± MAD (x106) Mean degree of frugivory (percentages) ± sd Frugivores interacting with native palms (group 1) 55 Euterpe edulis Geonoma pauciflora Allagoptera arenaria Syagrus romanzoffiana Attalea funifera Euterpe oleracea Geonoma elegans Geonoma schottiana 90 ± 96.67 2.81 ± 3.23 60.91 ± 24.59 Frugivores interacting with native and alien palms (group 2) 32 Livistona chinensis Archontophoenix cunninghamiana Elaeis guineensis 63.28 ± 50.74 7.58 ± 7.66 56.88 ± 29.67
Table 1. Summary statistics for two frugivore groups (group 1 & group 2) with the number or frugivore species, palm species, median and mean values for the investigated traits. For the two frugivore groups, the number of unique frugivore
species is given. The first row shows the native palm species frugivores interact with, the second row represents the alien palm species frugivores interact with. The distribution of traits values for body mass (in grams) and extent of occurrence (in km2) was right-skewed, therefore the median and median absolute deviation (MAD) are given. For degree of frugivory (in percentages of the total diet), the mean and standard deviation are given.
There was no significant difference in body mass between frugivore groups (Mann-Whitney U, N = 87, W = 1041, p = 0.1577) (figure 1a). This observation was in line with the expectation that body mass values would be similar for frugivores exclusively interacting with native palm species and frugivores that interact with both native and al palm species. Outliers in figure 1a showed a greater spread in body mass values for frugivores that feed on native palm species only. This trend was also observed when comparing the shape of the distribution (coloured area in figure 1a) as reflected in the median and MAD values (table 1); frugivore group 2 had relatively more individuals with a small body mass (M = 63.28, MAD = 50.74) than frugivore group 1 (M = 90, MAD = 96.67).
Figure 1. (a) Distribution of body mass (in grams) and (b) extent of occurrence (in km2) for two frugivore groups. The blue
colour indicates the distribution of frugivore group 1, the green colour indicates the distribution of frugivore group 2. The boxplot shows the summary statistics with the minimum, 1st quartile, median, 3rd quartile and maximum values. Datapoints
that fall outside the maximum range of the boxplot are visualized as black dots. (a) The body mass data for the native frugivore group had two outliers outside of the graph range that are represented as black dots with corresponding values.
In line with the expectations, there was a significant difference in extent of occurrence (in x106 km2) between frugivore groups (Mann-Whitney U, N = 87, W = 489, p < 0.001) with the frugivores interacting with both native and alien palm species having the largest extent of occurrence (Median = 7.58, MAD = 7.66) and the frugivores interacting with native palm species having the smallest (M = 2.81, MAD = 3.23). Figure 1b illustrates a larger, more even distribution of extent of occurrence for frugivore group 2. On the contrary, the extent of occurrence of the frugivore group 1 showed a more right-skewed distribution with relatively more individuals having a smaller extent of occurrence. This trend was also reflected in the MAD values in table 1 indicating a larger distribution for frugivore group 2 and a smaller distribution for frugivore group 1.
Contrary to the expectation, degree of frugivory did not differ significantly between the two frugivore groups (Mann-Whitney U, N = 87, W = 923.5, p = 0.702). In figure 2, the degree of frugivory is presented as the average proportion of the diet that is constituted of fruits and seeds. The boxplots in figure 2 clearly illustrate that median values and data distribution for the degree of frugivory were similar for both frugivore groups. The similarity of spread in degree of frugivory is also reflected in group means and standard deviations for frugivore group 1 and 2 (Mean = 60.91, sd = 24.59 and M = 56.88, sd = 29.67) (table 1). Analysis of the individual components of the diet, fruits and seeds also showed that both frugivore groups do not differ significantly (Mann-Whitney U, N = 87, W = 855.5, p = 0.8315 and W = 1009.5, p = 0.1488).
Figure 2. Average proportion (in percentages) of the total diet of frugivores for three diets. The blue colour indicates
frugivore group 1, the green colour indicates frugivore group 2. Boxplots show the summary statistics with the minimum, 1st
quartile, median, 3rd quartile and maximum values. The black dots visualize datapoints that fall outside of the boxplot
maximum.
Discussion
With the use of data on palm-bird interactions in the Atlantic Forest, a comparative study of frugivore traits important for the formation of novel interactions was conducted for two groups of frugivores; (1) frugivore species exclusively interacting with native palm species and (2) frugivore species interacting with both native and alien palm species.
As hypothesized, body mass did not differ significantly between frugivore groups, indicating that alien palms were successful in attracting an assembly of frugivorous birds that resemble the total community of frugivorous birds in the Atlantic Forest. As reported in previous research, most frugivorous birds have small body sizes (Buckley et al., 2006; Fleming et al., 1987), which is also reflected in the results; both frugivore groups consist of many species with small body sizes and few species with larger body sizes. Invasion of an animal-dispersed palm species can only be successful if it is compatible with the ecological community present (Traveset & Richardson, 2014) and can form novel interactions with birds that have a small body mass, as has happened with the alien palms investigated. The fact that the fruits of the investigated palms were small is in line with previous findings that animal-dispersed alien plants often carry small fruits and are therefore more likely to invade new environments, because there are many potential dispersal agents present (Buckley et al., 2006; Gosper & Vivian-Smith, 2010).
In line with the expectations, extent of occurrence was significantly larger for frugivore species interacting with both native and alien palm species. These results infer that frugivore species
co-occurring with a high number plant species constitute a large part of the frugivores interacting with alien plant species. Frugivore species that co-occur with many native and alien plant species are often generalists and can constitute a large proportion of the frugivores interacting with alien palm species, as also confirmed in other studies (Jordaan et al., 2011; Palacio et al., 2016). However, extent of occurrence can only be used as a proxy for estimating the abundance of generalist frugivores interacting with palm species, it does not tell if and how many species of frugivores are in fact generalist species.
Nevertheless, interactions between alien plants and generalist frugivores might also be explained by fruit dependency in frugivorous birds, with obligate frugivores having a more generalized diet than more opportunistic species (Schleuning et al., 2011). Because they frequently move to new food sources (Holbrook & Smith, 2000) and often forage over large distances searching fruits (Schleuning et al., 2011), obligate frugivores are considered to feed on many different fruits, including those of alien plants. However, these earlier findings were not reflected in our results showing no significant difference in degree of frugivory between the frugivore groups, indicating that both groups of frugivores equally depend on fruits.
In view of the relationship between fruit dependency and diet generalization as proposed by Schleuning et al. (2011), the results of extent of occurrence and degree of frugivory might seem conflicting. However, the absence of expected fruit dependency in frugivore group 2 might be explained by the fact that the alien palm species investigated do not fruit off-season and therefore not enlarge fruit availability for frugivores when native fruit is scarce, as often observed in invasion of animal-dispersed plants (Debussche & Isenmann, 1990; Jose et al., 2013). Additionally, palms only make up a fraction of the total plant community in the Atlantic Forest and not all palm species have interaction data available. Considering this, it is likely that more observation and data compilation is needed to know how plant-frugivore co-occurrence, diet generalization, and diet dependency contribute to the formation of novel interactions. For now it can be concluded that novel interactions are shaped by frugivores that co-occur with many plant species, but are not necessarily obligate frugivores or highly dependent on fruits.
In conclusion, this case study used the most up-to-date data on palm-bird interactions to investigate how frugivore traits contribute to the formation of novel interaction between frugivores and alien palm species in the Atlantic Forest. Results showed that the presumption of frugivore community compatibleness with introduced palm species was confirmed and that novel interactions are shaped by frugivores co-occurring with many plant species, but are not necessarily highly fruit dependent.
In addition to other research that studied differences in native and alien plant traits (Hulme & Bernard-Verdier, 2018; Ordonez et al., 2010) and studies on plant-frugivore interactions (Bender et al., 2018; Deckers et al., 2008), this study showed that comparative analysis of frugivore traits is a useful tool to assess the importance of frugivore communities in the formation of novel interactions. Greater understanding of frugivore interactions has led to the quantification of ecosystem wide plant-frugivore networks (Bender et al., 2018; Muñoz et al., 2019), a greater understanding of animal-mediated plant invasions (Traveset & Richardson, 2014) and the creation of invasion management frameworks (Pejchar & Mooney, 2009; Sheley et al., 2010). Knowledge on the contribution of frugivore traits in the formation of novel interactions remains crucial to understand the importance of frugivore communities in dispersing introduced plants (Buckley et al., 2006). Future comparative analysis of frugivore traits may provide increasing knowledge on plant-frugivore interactions and will prove important in understanding what shapes community networks and ecosystem functioning in tropical forests around the world.
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