Effects of urbanization on direct and indirect interactions in a tri‐trophic system

Abstract

While effects of urbanization on species assemblages are receiving increasing attention, effects on ecological interactions remain largely unexplored. We investigated how urbanization influences the strength of direct and indirect trophic interactions in a tri- trophic system. In a field experiment including five cities and nearby farmed areas, we used potted Vicia faba plants and manipulated the presence of Megoura viciae aphids and that of naturally occurring aphid predators. When predators could access aphids, they reduced their abundance less in the urban than in the agricultural ecosystem. Compared to aphid abundance on plants without predator access, abundance on plants with predator access was 2.58 times lower in urban and 5.27 times lower in agricultural areas. This indicates that urbanization limited top-down control of aphids by predators. In both ecosystems, plant biomass was negatively affected by herbivores and positively affected by predators, but the positive indirect predator effect was weaker in cities. Compared to aphid-infested plants without predator access, plants with predator access were 1.89 times heavier in urban and 2.12 times heavier in agricultural areas. Surprisingly, differences between ecosystems regarding the indirect predator effect on plants were not explained by the differentially strong herbivore suppression. Instead, the urban environment limited plant biomass per se, thereby mitigating the scope of a positive predator effect. Our results show that urbanization can influence direct and indirect trophic interactions through effects on biotic top-down forces and on plant growth. In order to understand how urbanization affects biodiversity and ecosystem functioning, it is fundamental to not only consider species assemblages, but also species interactions.

Does urbanization explain differences in interactions between an insect herbivore and its natural enemies and mutualists?

“…Urbanization is arguably the greatest anthropogenic transformation that ecological systems experience, and while most studies of urban ecology focus on changes to the diversity and abundance of species inhabiting towns and cities, attention has only started to focus on how assemblages of interacting species are formed in urban areas, and how this is affected by the intensity of urbanization (Bennett and Gratton 2012;Quispe and Fenoglio 2015;Pereira-Peixoto et al 2016;Turrini et al 2016). Fragmentation reduces populations of native plants (Benitez-Malvido 1998;Jules 1998;Williams et al 2005), leads to decreased connectivity between vegetation patches and existing patches tend to be smaller (Medley et al 1995;McKinney 2002) and therefore of reduced quality as habitat for many animal species (Bradley and Altizer 2007;Faeth et al 2011;Turrini et al 2016). There are also some dramatic physical changes from increased densities of roads, buildings and other sealed structures and microclimatic changes such as the urban heat island effect (Bradley and Altizer 2007;Faeth et al 2011).…”

“…Few studies have considered how these changes influences the outcome of ecological interactions at multiple trophic levels (Shrewsbury and Raupp 2006;Bennett and Gratton 2012;Fenoglio et al 2013;Pereira-Peixoto et al 2016;Turrini et al 2016). For example, abiotic environmental factors might interfere with biotic interactions, thereby modulating the strength of the trophic effects on food webs (Ritchie 2000;Preisser and Strong 2004;Turrini et al 2016). Mooney et al (2016) investigated if variation in light availability (shaded understory or open meadow) determines the abundance of the aphid Aphis helianthi feeding on the herb Ligusticum porteri.…”

“…If we consider that urban wildlife is subject to multiple changes in abiotic conditions simultaneously, it is not surprising that predicting the consequences of such changes for trophic processes and for direct and indirect species interactions is highly challenging (Turrini et al 2016). However, a few trends have begun to appear.…”

“…However, a few trends have begun to appear. Urban areas are often characterized by reduced numbers of native vertebrate predators (McKinney 2002;Shochat 2004), an increased abundance of some urban-adapted species, which can potentially lead to increased competition and displacement (Hostetler and McIntyre 2001), altered behavior and phenology (Connor et al 2002;Neil and Wu 2006), high densities of herbivorous arthropods (Dreistadt et al 1990;Hanks and Denno 1993;Tooker and Hanks 2000), lower numbers of arthropod predators (Turrini et al 2016) and lower numbers of parasitoids (Denys and Schmidt 1998;Bennett and Gratton 2012;Burks and Philpott 2017). All these changes can potentially lead to altered trophic structure, and we must recognize that trophic dynamics cannot be understood based only on our knowledge of species composition (Shochat et al 2006).…”

“…With direct trophic interactions such as predation, one species has a negative effect on the other species, but in indirect interactions one species can also positively affect another species through intermediate levels in a trophic cascade (Halaj and Wise 2001;Müller et al 2005;Turrini et al 2016). For example, the presence of some species of honeydewcollecting ants results in increased aphid numbers and also increased numbers of aphid parasitoids when protecting aphids from predators and incidentally also protecting parasitized aphids against predators and hyperparasitoids (Völkl 1992;Kaneko 2002).…”