Steve Garner
The Ecology of Fear: Trait-Mediated Indirect Interactions
Advanced Topics in Marine Ecology, Spring 2013
Extended Abstract
Indirect species interactions occur at all levels of an ecosystem, from the individual to the
community. Trait-mediated indirect interactions (TMIIs) are only a single type of indirect
interaction but comprise the major compliment to density mediated indirect interactions (DMIIs)
and in some examples play a greater role in shaping communities. Tri-trophic interactions (i.e.
between three species) result from consumer-resource interactions and subsequent chain effects.
It is important to distinguish the difference between TMIIs and DMIIs as DMIIs result from a
change in the number of individuals where as TMIIs refer to changes in behavior in response to a
stimulus, or lack there-of. The two are certainly intertwined and often confounded in that the
response behaviors exhibited by prey are intended to reduce predation (and maintain or increase
density) as far as compensatory declines in energy allocation will allow (Lima and Bednekoff,
1999). Despite selective pressures for favorable traits, individuals show a great deal of
phenotypic plasticity in terms of both potential and realized behavioral responses. Here I review
the literature relevant to the discussion of TMIIs, provide specific examples of several
behaviorally mediated trophic interactions, and discuss the comparative importance of TMIIs to
ecosystems using experimental evaluations of effect size.
Abrams (1995), followed later by Dill et al. (2003) and Werner and Peacor (2003), defined
TMIIs in terms of a three species food chain: “a species (the “initiator” of the effect) has a direct
effect on another (the “receiver” of the effect) if a change in some property of the initiator
species produces a change in a property of the receiver, and this change does not require a
change in any property of any other species to occur.” However, “effects are indirect if a change
in some property of another species (the “transmitter”) are caused by the change in the initiator’s
property and are required to produce the change in the property of the receiver species.” This
somewhat cumbersome definition can be visualized in Figure 1 taken from Dill et al., (2003). For
example (of many), the presence of a prey species initiates the presence of a predator species
which transmits an indirect effect of avoidance to a different potential prey species receiving the
effect. Dill et al. (2003) expand on TMIIs by providing some examples of various types such as
“competitor facilitation”, “apparent competition”, and “behavioral resource depression”. During
“competitor facilitation” the presence of a predator (initiator) affects the behavior of its prey
(transmitter) and causes that same prey to be more available to a competing predator species
(receiver). A great example of this type of interaction occurs when large predators (i.e. dolphins
and tunas) condense bait fish and force them to the surface where they become available to birds.
In the context of Abrams work in the optimal foraging arena, facilitation-type TMIIs occur when
the transmitter (prey) sacrifices foraging for refuge in the presence of the initiator (predator)
thereby reducing predation on the prey species (receiver) of the transmitter (Dill et al. 2003;
Griffin et al., 2012). More generally, any combination of three species in which species A feeds
on species B and species B feeds on species C likely exhibit some degree of TMII in response to
the presence of their respective predator species (either A or B or both).
Abrams (e.g. 1984, 1990, and 1991) intensively explored the importance of direct versus indirect
interactions in the context of optimal foraging theory, suggesting indirect effects would have a
greater impact on long-lived species with iteroparous reproductive strategies. Abrams (1984)
assumed that more active foragers are more vulnerable to predation and thus, the functional
response of a species is dependent upon its adaptive behavior potential. Walters et al., (1981)
demonstrated the ability to condition a succession of survival responses in the gastropod Apylsia
californica to non-predatory cues, showing that even prey with relatively simple nervous systems
are able to develop associations with negative stimuli. Investigations by Huang and Sih (1990)
further demonstrated the importance of behavioral responses in consumer-resource dynamics. In
a three species, one predator food-web (green sunfish, larval salamanders, and isopods) Huang
and Sih (1990) determined that the presence of isopods increased the foraging activity of green
sunfish (independent of density) which in turn increased refuge use by larval salamanders;
without the presence of isopods the change in larval salamander refuge use in the presence of
green sunfish was non-significant. They also found evidence of sexually dimorphic interspecies
interactions, which they termed “indirect antagonism,” where increased refuge use by larval
salamanders displaced female isopods from refuges making them more vulnerable to predation
(Huang and Sih, 1990). Male isopods were much more active and were unaffected by the
presence of salamanders. Chemical cues are the predominant initiators of response in both
predators and prey, with hydrodynamics playing a key role in the ability of predators to detect
prey scent trails (Weissburg and Zimmer-Faust, 1993). Favorable hydrodynamics result in
quicker, more successful searches while turbulence and stagnation may completely prevent prey
plume detection (Figure 2; Weissburg and Zimmer-Faust, 1993).
Community-level responses are thought to be heavily dependent on the densities of species and
their direct interactions. For example, predators may switch to a prey source when higher
densities increase capture efficiency, and thereby reducing predation on that prey’s own prey.
Certainly, TMIIs and DMIIs are intertwined as predators respond to changes in abundant prey,
but several studies have found effect sizes associated with TMIIs much larger than those
attributable to density only (Huang and Sih, 1990; Turner and Mittlebach, 1990; Wissinger and
McGrady, 1993; Werner and Peacor, 2003). Werner and Peacor (2003) cited several examples:
in a three species food web (Tramea->Erythmia->damselfly) the removal of the feeding
apparatus of top predator dragonfly larvae (Tramea) resulted in a 61% decrease in predation
upon damselflies by Erythemis, the primary prey of Tramea (Wissinger and McGrady, 1993),
where as only a 21% decrease was observed without manipulation (density only effect). As
mentioned above, Huang and Sih (1990) found TMIIs associated with sunfish, salamander larvae
and isopods, with the effect size of the TMII 2.4 times greater than that attributable to density
effects alone. Behavioral variability can disrupt seemingly simple experimental manipulations of
short, linear food webs, preventing scientists from differentiating controlling factors from
confounding effects. However, understanding behavioral interactions between predators,
competitors, and prey helps clarify the functional role of various species in food webs rather than
dismissing behavior as problematic uncertainty. The literature reviewed here clarifies the role of
indirect interactions using sound experiments and emphasizes the importance of behavioral
plasticity in shaping communities at the individual, genetic, and species levels.
Literature Cited
Abrams, P.A. 1984. Foraging time optimization and interactions in food webs. The American
Naturalist. 124(1): 80-96
Abrams, P.A. 1990. The effects of adaptive behavior on the type-2 functional response. Ecology.
71(3): 877-885
Abrams, P.A. 1991. Strengths of indirect effects generated by optimal foraging. Oikos. 62(2):
167-176
Abrams, P.A. 1992. Predators that benefit prey and prey that harm predators: unusual effects of
interacting foraging adaptations. The American Naturalist. 140(4): 573-600
Abrams, P.A. 1995. Implications of dynamically variable traits for identifying, classifying and
measuring direct and indirect effects in ecological communities. The American
Naturalist. 146: 112-134
Dill, L.M., M.R. Heithaus, C.J. Walters. 2003. Behaviorally mediated indirect interactions in
marine communities and their conservation implications. Ecology. 84(5): 1151-1157
Griffin, B.D., B.J. Toscano, J. Gatto. The role of individual behavior type in mediating indirect
interactions. 93(8): 1935-1943
Huang, C. and A. Sih. 1990. Experimental studies on behaviourally mediated, indirect
interactions through a shared predator. Ecology. 71(4): 1515-1522
Lima, S.L. and P.A. Bednekoff. 1999. Temporal variation in danger drives antipredator
behavior: the predation risk allocation hypothesis. The American Naturalist. 153(6): 649659
Soluk, D.A. and N.C. Collins. 1988. Synergistic interactions between fish and stoneflies:
facilitation and interference among stream predators. Oikos. 52: 94-100
Turner, A.M. and G.G. Mittlebach. 1990. Predator avoidance and community structure:
interactions among piscivores, planktivores, and plankton. Ecology. 71: 2241-2254
Walters, E.T., T.J. Carew, E.R. Kandel. 1981. Associative learning in Apylsia: evidence for
conditioned fear in an invertebrate. Science. 211(4481): 504-506
Weissburg, M.J. and R.K. Zimmer-Faust. 1993. Life and death in moving fluids: hydrodynamic
effects on chemosensory-mediated predation. Ecology. 74(5): 1428-1443
Werner, E.E. and S.D. Peacor. 2003. A review of trait-mediated indirect interactions in
ecological communities. Ecology. 84(5): 1083-1100
Wissinger, S. and J. McGrady. 1993. Intraguild predation and competition between larval
dragonflies: direct and indirect effects of shared prey. Ecology. 74: 207-218
Figures
Figure 1. Illustration of the response of the “receiver” (bottlenose dolphins) to the presence of the
“transmitter” (tiger shark) whose presence is in response to the “initiator” (dugong) exceeding
some threshold density in seagrass habitat. The “receiver” responds by reducing foraging in
shallow habitats despite high food availability in favor of predator avoidance (Dill et al., 2003).
Figure 2. Interactive effects of olfaction and hydrodynamics in mediating predation success. (A)
Predatory success and search path efficiency as a function of flow speed. (B) Initial locomotory
trajectories of unsuccessful searchers, and of crabs n the absence of prey, as a function of flow
speed. The highest success rate in intercepting a plume occurs at low flow (1 cm/s).