Non‐consumptive effects of avian predators on fish behavior and cascading indirect interactions in seagrasses

Abstract

Top–down impacts of avian predators are often overlooked in marine environments despite evidence from other systems that birds significantly impact animal distribution and behavior; instead, birds are typically recognized for the impacts of their nutrient rich guano. This is especially true in shallow seagrass meadows where restoration methods utilize bird perches or stakes to attract birds as a passive fertilizer delivery system that promotes the regrowth of damaged seagrasses. However, this method also increases the local density of avian piscivores that may have multiple unexplored non‐consumptive effects on fish behavior and indirect impacts to seagrass communities. We utilized laboratory and field experiments to investigate whether visual cues of avian predators impacted the behavior of the dominant demersal fish in seagrass habitats, the pinfish Lagodon rhomboides, and promoted cascading interactions on seagrass‐associated fauna and epiphytes. In laboratory mesocosms, pinfish displayed species specific responses to models of avian predators, with herons inducing the greatest avoidance behaviors. Avoidance patterns were confirmed in field seagrass meadows where heron models significantly reduced the number of fish caught in traps. In a long term field experiment, we investigated whether avian predators caused indirect non‐consumptive effects on seagrass communities by monitoring fish abundances, invertebrate epiphyte grazers, and the seagrass epiphytes in response to heron models, bird exclusions, and bird stakes. On average, more fish were recovered under bird exclusions and fewer fish under heron models. However, we found no evidence of cascading effects on invertebrate grazers or epiphytes. Bird stake treatments only displayed a simple nutrient effect where higher bird abundances resulted in higher epiphyte biomass. Our results indicate that although birds and their visual cues can affect fish and epiphyte abundance through non‐consumptive effects and nutrient enrichment, these impacts do not propagate beyond one trophic level, most likely because of dampening by omnivory and larger scale processes.

Effects of predator exposure on baseline and stress‐induced glucocorticoid hormone concentrations in pumpkinseedLepomis gibbosus

“…Similarly, a model osprey flying overhead resulted in significant behavioural modifications in nesting pumpkinseed Lepomis gibbosus (L. 1758), where the majority of predator‐exposed paternal fish temporarily abandoned their nests to find refuge away from the threat (Gallagher et al ., ). These insights, along with others (Hill & Heck, ; Pepino et al ., ; Steinmetz et al ., ), suggest that avian predators may exert top‐down influences on fish populations. However, the effects of avian predation on the physiological stress response of fish remains poorly characterised.…”

Avian predators transmit fear along the air–water interface influencing prey and their parental care

“…can affect fish distribution (Ryan et al 2013) and behavior and survival (Hill and Heck 2015;Pepino et al 2015).…”

“…Although many terrestrial and avian predators kill and consume aquatic prey (e.g., Dalton et al 2009), the nonconsumptive effects of these interactions remain relatively understudied, particularly for large bird predators (Fauchald and Erikstad 2002;Steinmetz et al 2003;Zydelis and Kontautas 2008; but see recent work by Hill and Heck 2015;Pepino et al 2015). Here we used a realistic model of an Osprey (Pandion haliaetus (L., 1758)), a predatory fish specialist throughout most of its range, to test the hypothesis that the presence of aerial predators can significantly alter fish parental behavior.…”

Seagrass Ecosystems: A career-long quest to understand their inner workings

“…The last post-doc who came to DISL and worked with me was Jennifer Hill. Jenn carried out interesting studies of predator-prey behavior (Hill and Heck 2015) and later with Sea Grant support investigated the impact of the non-native tiger shrimp (Penaus monodon) on the native shrimp species of the Gulf of Mexico (Hill et al 2017).…”