Density-dependent indirect effects: apparent mutualism and apparent competition coexist in a two-prey system

Abstract

A predator consuming multiple prey species usually causes indirect effects. Apparent mutualism results when multiple prey species reduce predation risk for each other by altering a predator's functional response. Short-term apparent competition occurs when multiple prey species increase predation risks for each other through the numerical response, i.e. increasing the predator's birth rate, or aggregative response, i.e. attracting a higher density of predators. Our objectives in this study were to determine the aggregative response and 2-prey functional response of a predator and to examine indirect effects over a range of prey densities. We used the clam Macoma balthica and juvenile blue crabs Callinectes sapidus as prey for adult blue crabs. In laboratory experiments, we determined the single-prey functional responses of the crabs to each prey species and the 2-prey functional response. We combined the 2-prey functional response with the known blue crab aggregative response to clams to estimate field predation rates. Our model predicts that at low prey densities, clams and juvenile blue crabs exhibit apparent mutualism, whereas at high clam densities, this relation switches to short-term apparent competition. These unexpected results highlight the need to incorporate multiple aspects of predation at multiple scales when considering indirect effects.KEY WORDS: Predator-prey interactions · Functional response · Indirect effects · Blue crab · Macoma balthicaResale or republication not permitted without written consent of the publisher Mar Ecol Prog Ser 456: 139-148, 2012 increases the predator density (i.e. changes either the predator's numerical or aggregative response), thus increasing predation on the other species (Holt & Lawton 1994). This occurs either through increasing the predator population growth rate (Settle et al. 1996, Carvalheiro et al. 2008 or through a local increase in predator density due to predator movement (Holt & Kotler 1987, Brown & Mitchell 1989, Murakami & Nakano 2002. Study organismsThe blue crab Callinectes sapidus Rathbun, 1896, is an important benthic predator in Chesapeake Bay (Virnstein 1977). Large adult crabs are opportunistic omnivores, feeding primarily on bivalves (~50% of diet) and crustaceans (~30%) as well as fish and polychaetes (Hines et al. 1990). Blue crabs are cannibalistic, with adults feeding on juveniles (Hines & Ruiz 1995). Because cannibalism represents a major source of mortality for juvenile blue crabs, juveniles congregate in shallow waters (<1 m), where adults are less abundant (Hines & Ruiz 1995, and in structured habitats that provide a predation refuge (Everett & Ruiz 1993).Macoma balthica Linnaeus, 1758, is a small (shell length < 40 mm) tellinid clam that is the dominant biomass in unvegetated mud habitats within the mesohaline regions of Chesapeake Bay (Holland et al. 1977) and is a major source of food for blue crabs (Baird & Ulanowicz 1989). M. balthica avoids predation by burying deeply, up to 35 cm, in the sediment (Hines & Comtois 1985)...

Invasive rodents have multiple indirect effects on seabird island invertebrate food web structure

“…Less diversity among these tertiary and secondary consumers can decrease competition within these trophic levels, ultimately decreasing the diversity of prey due to decreased apparent mutualisms (in line with the principle that “the predator/competitor of my predator is my friend”; Abrams , Abrams and Matsuda , Long et al. ). This decrease in prey diversity would finally serve to increase the competition between predators, decreasing the persistence of less competitive predator species (Kratina et al.…”

“…We argue that the inverse may be occurring on invaded islands: lower foliar (and leaf litter) nutrients will lead to lower abundance and nutrient content of primary consumers, which in turn leads to the decline of secondary and tertiary consumer diversity. Less diversity among these tertiary and secondary consumers can decrease competition within these trophic levels, ultimately decreasing the diversity of prey due to decreased apparent mutualisms (in line with the principle that "the predator/competitor of my predator is my friend"; Abrams 1987, Abrams and Matsuda 1996, Long et al 2012. This decrease in prey diversity would finally serve to increase the competition between predators, decreasing the persistence of less competitive predator species (Kratina et al 2007, Hammill et al 2015, and further decreasing the number of species the ecosystem can support.…”

Individual, population, and ecosystem effects of hypoxia on a dominant benthic bivalve in Chesapeake Bay

“…As the densities of these prey decrease, the proportional mortality decreases, so the prey have a low-density refuge from predation. The functional response can be changed both qualitatively and quantitatively by changes in habitat (Lipcius and Hines 1986, Dittel et al 1995, Long et al 2012b, predator size and density (Mansour andLipcius 1991, Gonza´lez-Sua´rez et al 2011), the presence and density of alternative prey (Chesson 1989, Long et al 2012a, and the spatial arrangement of prey (Hines et al 2009, Long andHines 2012). Blue crabs have a type III FR toward M. balthica (Eggleston et al 1992, Taylor andEggleston 2000), but as hypoxia should decrease predator search time for M. balthica, we hypothesized that it may change the FR from a type III to a type I or II.…”

Hidden layers of density dependence in consumer feeding rates

“…In contrast, our results indicate that one would almost always need to know the characteristics of the consumers and resources before being able to adequately describe feeding rates. Moreover, a given consumer's feeding rate could just as easily appear consistent with one model for a first resource and with a different model with regard to another (e.g., Long et al, 2012a) or, worse yet, somewhere in between (e.g., Lester & Harmsen, 2002). Clearly, more empirical work is needed to understand the biology that determines why any given consumer-resource-resource combination lands in one particular location along the spectra of process inter-dependencies, particularly in the context of predators that feed on more than just two prey species.…”