An experimental test of how parasites of predators can influence trophic cascades and ecosystem functioning

Abstract

Parasites can shape the structure and function of ecosystems by influencing both the density and traits of their hosts. Such changes in ecosystems are particularly likely when the host is a predator that mediates the dynamics of trophic cascades. Here, we experimentally tested how parasite load of a small predatory fish, the threespine stickleback, can affect the occurrence and strength of trophic cascades and ecosystem functioning. In a factorial mesocosm experiment, we manipulated the density of stickleback (low vs. high), and the level of parasite load (natural vs. reduced). In addition, we used two stickleback populations from different lineages: an eastern European lineage with a more pelagic phenotype (Lake Constance) and a western European lineage with a more benthic phenotype (Lake Geneva). We found that stickleback caused trophic cascades in the pelagic but not the benthic food chain. Evidence for pelagic trophic cascades was stronger in treatments where parasite load of stickleback was reduced with an antihelmintic medication, and where fish originated from Lake Constance (i.e., the more pelagic lineage). A structural equation model revealed that differences in stickleback lineage and parasite load were most likely to impact trophic cascades via changes in the composition, rather than overall biomass, of zooplankton communities. Overall, our results provide experimental evidence that parasites of predators can influence the cascading effects of fish on lower trophic levels with consequences on ecosystem functioning.

Parasites as conservation tools

“…The cascading effects of parasitic reduction on ecosystems were experimentally tested in threespine stickleback ( Gasterosteus aculeatus ). Parasite reduction increased survival of the fish resulting in trophic cascades and declines in primary producers (Anaya‐Rojas et al., 2019). Parasites can change the behavior of intermediate hosts and their availability to higher trophic levels (Sato et al., 2019; Wood & Johnson, 2015).…”

“…Infection with the nematode Trichostrongylus tenuis affects the reproductive output and winter survival of Red Grouse (Lagopus lagapus scoticus) and results in selective predation by canids (Hudson et al, 1992). The cascading effects of parasitic reduction on ecosystems were experimentally tested in threespine stickleback (Gasterosteus Parasite reduction increased survival of the fish resulting in trophic cascades and declines in primary producers (Anaya-Rojas et al, 2019). Parasites can change the behavior of intermediate hosts and their availability to higher trophic levels (Sato et al, 2019;Wood & Johnson, 2015).…”

The opposing roles of lethal and nonlethal effects of parasites on host resource consumption

“…Over the past 10 years, there has been great effort to place parasites into food webs (Byers, 2009 ; Hatcher et al, 2012 ; Lafferty et al, 2008 ) and broader ecological theory (Buck & Ripple, 2017 ; Daversa et al, 2021 ; Dunn et al, 2012 ; Raffel et al, 2008 ; Thomas et al, 2005 ). Specifically, recent work has drawn parallels between parasite–host and predator–prey literature such as trophic cascades, indirect effects, and nonlethal effects (Anaya‐Rojas et al, 2019 ; Buck, 2019 ; Buck & Ripple, 2017 ; Daversa et al, 2021 ; Dunn et al, 2012 ; Raffel et al, 2008 ). Parasites, like predators, can have lethal effects on their hosts, as well as cause trait responses in their hosts that result in nonlethal effects.…”

What doesn’t kill you doesn’t make you stronger: Parasites modify interference competition between two invasive amphipods

“…This includes such aspects as morphology (Bakker et al 1997), habitat selection (Żbikowska and Cichy 2012;Rachalewski et al 2018), mobility (Dezfuli et al 2003), boldness (Flegr 2015), aggression (Thomas et al 2005;Mikheev et al 2010), foraging (Fielding et al 2003;Bącela-Spychalska et al 2014) and reproduction (Hall et al 2007). These changes may further propagate to the impact on ecosystem functioning (Friesen et al 2017;Anaya-Rojas et al 2019) through intra-and interspecific interactions of infected individuals with other organisms through consumption (Fielding et al 2003), predation (Bakker et al 1997;Flegr 2015;Friesen et al 2019) or competition (Anderson and May 1986;Mikheev et al 2010;Reisinger et al 2015;Friesen et al 2018).…”