Trophic cascade within and across ecosystems: the role of anti-predatory defenses, predator type, and detritus quality

Abstract Species in one ecosystem can indirectly affect multiple biodiversity components and ecosystem functions of adjacent ecosystems. The magnitude of these cross-ecosystem effects depends on the attributes of the organisms involved in the interactions, including traits of the predator, prey and basal resource. However, it is unclear how predators with cross-ecosystem habitat interact with predators with single-ecosystem habitat to affect their shared ecosystem. Also, unknown is how such complex top-down effects may be mediated by the anti-predatory traits of prey and quality of the basal resource. We used the aquatic invertebrate food webs in tank bromeliads as a model system to investigate these questions. We manipulated the presence of a strictly aquatic predator (damselfly larvae) and a predator with both terrestrial and aquatic habitats (spider) and examined effects on survival of prey (detritivores grouped by anti-predator defense), detrital decomposition (of two plant species differing in litter quality), nitrogen flux and host plant growth. To evaluate the direct and indirect effects of each predator type on multiple detritivore groups and ultimately on multiple ecosystem processes, we used piecewise structural equation models. For each response variable, we isolated the contribution of different detritivore groups to overall effects by comparing alternate model formulations. Alone, damselfly larvae and spiders each directly decreased survival of detritivores and caused multiple indirect negative effects on detritus decomposition, nutrient cycling, and host plant growth. However, when predators co-occurred, the spider caused a negative non-consumptive effect on the damselfly larva, diminishing the net direct and indirect top-down effects on the aquatic detritivore community and ecosystem functioning. Both detritivore traits and detritus quality modulated the strength and mechanism of these trophic cascades. Predator interference was mediated by undefended or partially defended detritivores as detritivores with anti-predatory defenses evaded consumption by damselfly larvae but not spiders. Predators and detritivores affected ecosystem decomposition and nutrient cycling only in the presence of high-quality detritus, as the low-quality detritus was consumed more by microbes than invertebrates. The complex responses of this system to predators from both recipient and adjacent ecosystems highlight the critical role of maintaining biodiversity components across multiple ecosystems. 
MethodsBetween January and March 2010 (35 days), we manipulated predators and detritivores within bromeliads settled within experimental cages. Each cage consisted of a rectangular wire frame (0.50m × 0.60m) covered with a white fabric mesh that allowed moderate light to pass through, fixed to the top edge of a pot into which the experimental bromeliad was planted. An emergence trap, made of an inverted plastic bottle, was placed on top of each cage to capture adults of detritivores that emerged during the experiment. We randomly arranged these 48 bromeliads into 12 blocks of four bromeliads, with a minimum distance of 20 meters between blocks. We randomly assigned each block to the following treatments: (i) only detritivores, without predators (control treatment); (ii) detritivores + damselfly larva; (iii) detritivores + spider; (iv) detritivores + damselfly larva + spider. We used an additive design, in which the density of each predator species is held constant since this design, unlike a substitutive design, avoids confounding the absolute effect of interspecific interactions (in the predator co-occurrence treatment) with intraspecific interactions (Sih et al.1998; Romero & Srivastava, 2010). This allows us to assess predator impact regarding individual and multiple effects (i.e., considering potential interspecific interactions between spider and damselfly larvae). Prior to the inclusion of the organisms, we added portions of approximately 15 previously dried and weighed leaves of Eugenia uniflora (Myrtaceae) (mean = 0.24g; SD ± 0.002g) and of Ocotea pulchella (Lauraceae) (mean = 0.57g; SD ± 0.009g) distributed equally among the bromeliad tanks. The litter of both plant species is commonly found inside the bromeliad tanks in the study area. We consider E. uniflora to be the higher quality litter for two reasons: (1) it has higher specific leaf area than O. pulchella, (97.77 cm2.g-1 ± 27.3, Migliorini et al., 2018; and 67.9 cm2.g-1 ± 5.0, Boerger & Wisniewski, 2003, respectively), often an indicator of higher palatability (Kurokawa et al., 2010; Schädler et al., 2003), which can also increase detrital decomposition rates (Migliorini et al., 2018); (2) it was fertilized with 15N in order to trace nitrogen flux from detritus to bromeliads.  Once the litter was added, we added ten chironomids, five culicids, three limoniids, three scirtids, and two trichopterans in each experimental plant. The abundance of...