bioRxiv preprint doi: https://doi.org/10.1101/340430; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Ecological network assembly: how the regional metaweb influences local food webs Leonardo A. Saravia 1 2 6, Tomás I. Marina 3, Nadiah P. Kristensen 5, Marleen De Troch 4, Fernando R. Momo 1 2 1. Instituto de Ciencias, Universidad Nacional de General Sarmiento, J.M. Gutierrez 1159 (1613), Los Polvorines, Buenos Aires, Argentina. 2. INEDES, Universidad Nacional de Luján, CC 221, 6700 Luján, Argentina. 3. Centro Austral de Investigaciones Científicas (CADIC-CONICET). 4. Marine Biology, Ghent University, Krijgslaan 281/S8, B-9000, Ghent, Belgium. 5. Department of Biological Sciences, National University of Singapore, 14 Science Drive 4 Singapore 117543, Singapore. 6. Corresponding author e-mail [email protected], ORCID https://orcid.org/0000-0002-7911- 4398 keywords: Metaweb, ecological network assembly, network assembly model, food web structure, modularity , trophic coherence, motif, topological roles, null models Running title: The metaweb influence on local food webs. 1 bioRxiv preprint doi: https://doi.org/10.1101/340430; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Abstract 1. Local food webs can be studied as the realization of a sequence of colonizing and extinction events, where a regional pool of species —called the metaweb— acts as a source for new species, these are shaped by evolutionary and biogeographical processes at larger spatial and temporal scales than local webs. Food webs are thus the result of assembly processes that are influenced by migration, habitat filtering, stochastic factors, and dynamical constraints. 2. We compared the structure of empirical local food webs to webs resulting from a probabilistic assembly null model. The assembly model had no population dynamics but colonization and extinction events with the restriction that consumer species have prey present. We use for comparison several network properties including trophic coherence, modularity, motifs, topological roles, and others. We hypothe- sized that the structure of empirical food webs should differ from model webs in a way that reflected dynamical stability and other local constraints. Three data sets were used: (1) the marine Antarctic metaweb, with 2 local food-webs (2) the 50 lakes of the Adirondacks; and (3) the arthropod community from Florida Keys’ classic defaunation experiment. 3. Contrary to our expectation, we found that there were almost no differences between empirical webs and those resulting from the assembly null model. Few empirical food webs showed significant differences with network properties, motif representations and topological roles, compared to the assembly null model. 4. Our results suggest that there are not strong dynamical or habitat restrictions upon food web structure at local scales. Instead, the structure of local webs is inherited from the metaweb without modifications. 5. Recently, it has been found in competitive and mutualistic networks that structures that are often attributed as causes or consequences of ecological stability are probably a by-product of the assembly processes (i.e. spandrels). We extended these results to trophic networks suggesting that this could be a more general phenomenon. Introduction What determines the structure of a food web? The characterization of ecological systems as networks of interacting elements has a long history (Paine, 1966; Robert M. May, 1972; Cohen & Newman, 1985); however, the effects of ecological dynamical processes on network structure are not fully understood. Structure is the result of community assembly, which is a repeated process of species arrival, colonization, and local extinction (Cornell & Harrison, 2014). That implies there are two major components that determine food 2 bioRxiv preprint doi: https://doi.org/10.1101/340430; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. web structure: the composition of the regional pool, from which the species are drawn; and a selective process that determines which species can arrive and persist in the local web. The selective process is very complex, involving multiple mechanisms (Mittelbach & Schemske, 2015). However, we should in theory be able to detect the signal of this process by comparing local webs to the regional pool from which they were drawn. The structure of a food web is ultimately constrained by the species and potential interactions that exist in the regional pool, i.e., the metaweb. The metaweb is shaped by evolutionary and biogeographical processes that imply large spatial and temporal scales (Carstensen, Lessard, Holt, Krabbe Borregaard, & Rahbek, 2013; Kortsch et al., 2018), and it generally extends over many square kilometers and contains a large number of habitats and communities (Mittelbach & Schemske, 2015). Importantly, the metaweb permits species co-occurrences and interactions that would be precluded by the selective process, which acts more strongly at local scales (Araújo & Rozenfeld, 2014). Therefore, comparing local webs to the metaweb may allow us to separate the larger evolutionary and biogeographical processes (Carstensen, Lessard, Holt, Krabbe Borregaard, & Rahbek, 2013; Kortsch et al., 2018) influencing food web structure from the theorized selective and local processes. More specifically, the assembly of local communities is influenced by dispersal, environmental filters, biotic interactions and stochastic events (HilleRisLambers, Adler, Harpole, Levine, & Mayfield, 2012). These processes have been studied using metacommunity theory, where different spatial assemblages are connected through species dispersal (Leibold, Chase, & Ernest, 2017). Recently, there has been an increase in food web assembly studies, integrating them with island biogeography (Gravel, Massol, Canard, Mouillot, & Mouquet, 2011), metacommunity dynamics (Pillai, Gonzalez, & Loreau, 2011; Liao, Chen, Ying, Hiebeler, & Nijs, 2016) and the effects of habitat fragmentation (Mougi & Kondoh, 2016). Which regional species can arrive and persist in a web is influenced by dispersal, environmental filters, biotic interactions and stochastic events (HilleRisLambers, Adler, Harpole, Levine, & Mayfield, 2012). These processes have been studied using metacommunity theory, where different spatial assemblages are connected through species dispersal (Leibold, Chase, & Ernest, 2017). Recently, there has been an increase in food web assembly studies, integrating them with island biogeography (Gravel, Massol, Canard, Mouillot, & Mouquet, 2011), metacommunity dynamics (Pillai, Gonzalez, & Loreau, 2011; Liao, Chen, Ying, Hiebeler, & Nijs, 2016) and the effects of habitat fragmentation (Mougi & Kondoh, 2016). As an extension of the species-area relationship (SAR) approach, one can derive a network-area relationship (NAR) using theoretical models (Galiana et al., 2018). However, this approach assumes that ecological dynamics (e.g., stability) will have no influence. 3 bioRxiv preprint doi: https://doi.org/10.1101/340430; this version posted April 22, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Compared to the body of theory, there are very few studies that have analyzed this process using experimental or empirical data, and none of them focuses on topological network properties that could be related to different assembly processes. Piechnik, Lawler, & Martinez (2008) found that the first to colonize aretrophic generalists followed by specialists, supporting the hypothesis that biotic interactions are important in the assembly process (Holt, Lawton, Polis, & Martinez, 1999). Baiser, Buckley, Gotelli, & Ellison (2013) showed that habitat characteristics and dispersal capabilities were the main drivers of the assembly. Fahimipour & Hein (2014) also found that colonization rates were an important factor. A key determinant of food web structure that has received a lot of theoretical attention is ecological dynamics, and particularly the role of dynamical stability (Robert M. May, 1972; McCann, 2000). Some theorists conceive of assembly as a non-Darwinian selection process (Borrelli, 2015), whereby species and structures that destabilize the web will be lost and stabilizing structures persist (Prill, Iglesias, & Levchenko, 2005; Pawar, 2009; Borrelli, 2015 ). Typically, assembly simulations produce large webs that are both stable in the dynamical sense and relatively resistant to further invasions (Drake, 1990; Luh & Pimm, 1993; Law & Morton, 1996). Therefore, we expect that particular structural properties that confer stability will be over-represented in real food webs (Borrelli et al., 2015), as these are the webs that are able to persist in time (Grimm,