Modularity of trophic network is driven by phylogeny and migration in a steppe ecosystem

Highlights

• Using the largest available trophic network of a large steppe ecosystem, we tested that steppe trophic networks including migratory species are associated with (i) migratory strategy and (ii) phylogenetic relatedness of interacting species.

• We found that (1) a substantial number of links were established by migrant taxa; (2) the phylogenetic signal in network structure was moderate for both consumer and prey nodes; (3) both consumer and prex phylogenies affected modularity, which was modulated by migration strategy; and (4) all species-level graph properties significantly differed between networks including and excluding migratory taxa.

• Our findigs provide information for conservation planning by identifying key trophic links in migratory taxa.

Abstract

Evidence is mounting that the structures of trophic networks are governed by migratory movements of interacting species and also by their phylogenetic relationships. Using the largest available trophic network of a large steppe ecosystem, we tested that steppe trophic networks including migratory species are associated with (i) migratory strategy and (ii) phylogenetic relatedness of interacting species: (1) whole graph-level metrics, estimated as modularity, and (2) species-level network metrics, measured as node degree (number of interacting partners), and centrality metrics. We found that (1) a substantial number of links were established by migrant taxa; (2) the phylogenetic signal in network structure was moderate for both consumer and prey nodes; (3) both consumer and prex phylogenies affected modularity, which was modulated by migration strategy; and (4) all species-level graph properties significantly differed between networks including and excluding migratory taxa. In sum, here we show that the structure of steppe trophic networks is primarily governed by migratory strategies and to a lesser extent, by phylogenetic relatedness, using the largest available food web representative for steppe ecology and migration biology.

Introduction

Organisms interact with each other to form highly structured complex networks, leading to ecological communities (Bascompte et al., 2003, Olesen et al., 2007, Thébault and Fontaine, 2010; Poisot et al., 2016). The architecture of these webs ranges from unnested to nested patterns of links, the analysis of which is important for the understanding of ecological, evolutionary and coevolutionary processes (e.g. Lewinsohn et al., 2006, Dormann et al., 2017, Pellissier et al., 2017, Tylianakis and Morris, 2017).

Specifically, numerous investigations of trophic network structure have detected that topology, strength and type of trophic interactions conform to a limited number of defining rules. For example, food webs have been shown to be key determinants of ecosystem functionality as their topology defines energetic processes and underpins key processes including network resilience (Loreau and Behera, 1999; Kéfi et al., 2015).

Trophic networks among species are not governed solely by species co-occurrences, but also by phylogenetic relatedness of interacting species. Therefore, phylogenetic signal inherent in food webs suggests that evolution plays a key role in determining community architecture and thus could deepen our understanding of the underlying mechanisms. (Peralta, 2016). Consequently, the investigation of such networks requires the consideration of the phylogenetic histories of both sets of participants in an ecological interaction (Hadfield et al., 2013; Rafferty and Ives, 2013). Theory predicts that closely related species are ecologically more similar to each other than expected based solely on the timing of their phylogenetic divergence, as a result of phylogenetic niche conservatism (Peterson et al., 1999). Indeed, niche conservatism has been demonstrated in numerous plants and animals, several ecological and life-history traits as well as network metrics (Freckleton et al., 2002, Qian and Ricklefs, 2004).

Recently, investigations of the properties of time-aggregated networks revealed that temporal dynamics should be considered in several ecological and evolutionary questions and consistently concluded that network analyses ignoring or not adequately accounting for temporal patterns might provide biased results (Blonder et al., 2012).

An important aspect of temporal changes in the composition of trophic networks is provided by the presence and absence of migratory animals. Indeed, Bauer and Hoye (2014) showed that migratory species forage and are preyed upon throughout their journeys, thereby establishing trophic interactions with other migrants and resident communities. Specifically, migrant and resident species are fundamentally different by the timing of their interactions, governing relationships between migrant abundance and primary production as well as the stability of trophic networks. Thus, presence and absence of migrants might substantially change the structure of food webs.

One of the primary ecological functionalities of grassland ecosystems include providing migratory hotspots for billions of migratory birds and insects, especially in steppe ecosystems with considerable amounts of wetland habitats (Sanderson et al., 2006; Zwarts et al., 2009). One of the key migratory hotspots for birds migrating along African-Palearctic flyways is represented by the Hortobágy steppe in East-Hungary, where up to 500,000 birds migrate on an annual basis, which is considered as the westernmost outpost of the Eurasian steppe zone (Chibilyev, 2002; Ecsedi, 2004).

Up to now, no published datasets are available which include information on trophic networks accounting for migration strategy and phylogeny. In our study we investigated the role of migration strategy and evolutionary relatedness on the temporal development of trophic network structure using the largest dataset of trophic links in a representative steppe ecosystem.

To do so, we hypothesized that network properties, which have been shown to be of relevance for characterising trophic networks including migratory species, are associated with (i) migratory strategy and (ii) phylogenetic relatedness of interacting species. The phylogenetic dependence was estimated applying (1) whole-level metrics, estimated as modularity, which has been shown to be present in virtually all ecological networks analysed so far (Dormann et al., 2017) and which is often related to phylogenetic patterns of ecological networks (Lewinsohn et al., 2006); (2) species-level network metrics, measured as node degree (number of interacting partners), and centrality metrics; Guimera and Amaral, 2005, Pavlopoulos et al., 2011).

To test these relationships, we calculated all of these network metrics for the Hortobágy network on a weekly scale and applied information theoretic approach to retrieve the relative importance of migration and phylogeny in governing food web topology.