Morphological defenses in marine systems: cost or benefit?
Whitney A. Scheffel
University of South Alabama, Dauphin Island Sea Lab, AL 36528
05-06-13
Predation plays a large role in prey behavior, life history traits, and population dynamics
and can ultimately have an effect on their morphological variation. Prey have developed
predator-resistant chemical, morphological and behavioral defenses to combat this stressor in
their associated environments. Morphological defenses in marine animals can be of benefit
when food resources are high in combination with predation stress. It can become a cost to the
animal when food resources and predation stress is low, causing them to be outcompeted by
more fit individuals. Predation affects morphology both directly and indirectly via reduced
growth and activity (Bourdeau and Johansson 2012; Figure 1). Defense production and
maintenance come at a cost when energy could be contributing to growth and reproduction
(Relyea and Auld 2005). Induced defenses tend to be more beneficial when predation intensity
is fluctuating and not consistent (Havel 1989; Bourdeau 2010). These defenses are induced by
two main environmental cues: predatory and injured conspecific (Appleton and Palmer 1988).
Judging by a majority of the studies performed in marine systems, prey response tends to be
the strongest when both of these cues are present (Bourdeau 2010). It is vital for a prey to be
able to accurately predict predator presence and risk in order to rapidly respond to the stressor
(Havel 1989). Induced defenses tend to evolve when the defensive structure is effective against
a single predator and the prey bearing the structure has a short generation time relative to the
speed with which the predator can reduce prey levels (Havel 1989).
An example of a predator-induced defense is that of the crucian carp (Carassius
carassius) in the Baltic Proper in response to the Northern pike (Esox lucius). Individuals are
able to increase their body depth in order to defend against the gape limited piscivore, E. lucius.
The crucian carp develop into a shallower bodied morph in the absence of the predator.
Pettersson and Brönmark (1997) performed experiments that investigated the performance of
each morph in both high and low densities with varying food levels to determine whether the
shallow bodied morph had a competitive advantage over the deep bodied morph. Results
showed that when pike were absent and food was in limited supply, deep bodied individuals
suffered a cost when competing with the shallow bodied morphs. In the high density
treatment, shallow bodied fish gained twice as much body mass as the deeper bodied fish.
Additional costs of this defense include increased drag when swimming which expends more
energy and increased basal metabolism. Once these fish reach a certain size refuge, they begin
to grow longer which indicates that this defense is somewhat reversible. Furthermore, another
fish species from the same region shows a different trend in terms of predator-induced
plasticity. Välimäki et al. (2012) performed experiments with the nine spined stickleback
(Pungitius pungitius) in response to perch (Perca fluviatilis) olfactory cues. When comparing
male and female fish from marine and freshwater pond populations amongst predator and
food level treatments, results suggest that females and marine fish express a stronger defense
response. They are more armored, streamline, and contain more lateral plates than freshwater
individuals in favorable food conditions (Välimäki et al. 2012). These results indicate that the
nine spined stickleback does not exhibit predator-induced plasticity in their body shape or
armor based on unreliable olfactory cues of the predatory perch. There is evidence for this
type of defense in the mimetic relationship between the tropical bridled burrfish
(Chilomycterus antennatus) and the unpalatable sea hare (Aplysia dactylomelia). Heck and
Weinstein (1978) observed this relationship in Panama where they collected post-larval burrfish
that resembled the more unpalatable sea hare. The burrfish is highly susceptible to predation
throughout its early life stages whereas the chemically defended sea hare has very few native
predators. This mimic allows them to quickly reach their adult stage where acquire protective
spines and the ability to inflate their bodies (Heck and Weinstein 1978).
Various marine invertebrates also express morphological defense mechanisms in
response to chemical cues of their associated predator and have been the focus of many
experimental studies (Lively 1986; Appleton and Palmer 1988; Bourdeau 2010; Moody and
Aronson 2012). The predatory snail (Acanthina angelica) induced a shell dimorphism response
by the intertidal acorn barnacle (Chthalamus anisopoma) with the two phenotypes being a
volcano shaped and a bent form (Lively 1986; Lively et al. 2000). This defense mechanism
became apparent after multiple settlement plate and dose-response experiments were
conducted. They wanted to test two central hypotheses: (1) A. angelica either induces the bent
morphology or attracts genetically determined larvae of the bent form; (2) exposing juvenile
barnacles to A. angelica would cause them to mature faster. Results indicated that there was a
mixture of inducible and non-inducible individuals within the same population. Non-inducible
individuals had lower predation risk and greater reproductive output when surrounded by the
inducible morph (Lively et al. 2000). The bent morph was induced by the predatory snail, but
showed no indication of early maturity, only faster growth.
Furthermore, examples of similar inducible plastic traits exist in three marine
gastropods, the marsh periwinkle (Littoraria irrorata), the frilled dogwinkle (Nucella lamellosa),
and the flat periwinkle (Littorina obtusata). Experimental tests were conducted to test if there
were changes in the shell morphology after being exposed to predatory cues and crushed
conspecifics. In the marsh periwinkle, there were novel findings of a significant increase in the
rate and production of labial ridge calcification when exposed to both conspecific cues and cues
from the predatory blue crab (Callinectes sapidus) (Moody and Aronson 2012). Trussell et al.
(1996; 2002) saw similar results in the response of the intertidal snail L. obtusata in the
presence of a common shore crab (Carcinus maenas). Snails produced thicker shells in both
wave exposed and protected shorelines when exposed to crabs. When similar experiments
were conducted with N. lamellosa, they developed larger apertural teeth when held in the
presence of the red rock crab (Cancer productus) (Appleton and Palmer 1988). The responses
were different for those exposed to crab effluent fed frozen fish and those that were fed thin
shelled snails. Those snails that developed the larger teeth fed less and also grew at a slower
rate (Appleton and Palmer 1988). This trait seems to be inducible with a genetic basis and
does not occur as often when predation risk is low due to its energetic cost. The final example
of a known inducible defense is that of the spine producing bryozoan (Membranipora
membranacea), a colonial organism found encrusted upon kelp blades fed upon by the cryptic
nudiranch (Doridella steinbergae) in the Pacific Northwest. Following a series of cue and
predation experiments, the production of spines by the attacked colony and the adjacent target
colony were greater at high nudibranch densities than those located some distance away. The
amount of zooids consumed per day was significantly less for spined individuals versus
unspined indicating the defense accurately deterred predation (Harvell 1986).
In conclusion, the results of these studies regarding both solitary and clonal organisms’
morphologies suggest that inducible defenses are preferred when predatory cues are reliable
and intermittent. These defenses may have energetic costs associated with them, but most
prove to be successful at deterring predation. More experimental evidence is needed to
document the relationship between prey activity, growth and defense production so we can
better understand the costs and benefits of these morphological changes in various marine
ecosystems.
References
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Figure 1: Flow chart of energy and direct and indirect (hatched arrows) effects of predation risk
on prey morphology. Predation can affect morphology indirectly through changes in prey
activity, growth, and stress response. Tradeoffs can occur with more allocation to growth
and development. (Bourdeau and Johansson 2012)