Predator vs. Prey: Predation and Fear for your life!

Marine Predators Top predators Upper level mesopredators Lower Level Mesopredators

Predation in Marine Communities Predation contributes to the structure of many marine communities through trophic cascades Predator Resource Prey Indirect Effect Direct Effect

Otters, Urchins, and Kelp Forests Estes,1978 Predation in Marine Communities

Blue crabs, Periwinkle Snails, Cordgrass Silliman and Bertness, 2002 Predation in Marine Communities Silliman Salt Marshes

Loss of Top Predators

Predator-Prey Arms Race Natural selection will – Favor predators that are efficient – And select for improvement in prey defenses to overcome predators A cycle and escalation of adaptations and counter- adaptations– an arms race!

Predator-Prey Arms Races Red Queen Evolution – “it takes all the running you can do to keep in the same place” – Without constant evolution, you would be eaten!

Why is it that the arms race is always slightly in favor of the prey? – Life dinner principle- the rabbit is running for his life while the fox is only running for his dinner’ Dawkins 1979 It’s a lots more important to avoid being eaten than it is to miss a meal! Predator-Prey Arms Races

Temporal trends in bite mark frequencies on Mesozoic motile and sessile crinoids (A). Predator-Prey Arms Races

Don’t eat me! Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage Used by many marine organisms – The master of camouflage The master of camouflage

Don’t eat me! Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage Can be visual

Don’t eat me! Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage Often visual

Camouflage Polymorphic cryptic coloration – Different color morphs exist within a population May prevent predators from developing a search image Search Image

Camouflage Palma and Steneck, 2001 – Polychromatic variations enhance survival in polychromatic habitats

Don’t eat me! Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage Or chemical – Decorator crabs

Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage – 2) Warning Coloration-Aposematism Bright colors become associated with defended animals – Has evolved independently multiple times Don’t eat me!

Aposematism Common in marine nudibranchs

Aposematism Conspicuous colors help predators to learn to avoid unpalatable prey and may help to reduce recognition errors

Aposematism Fish learn to avoid distasteful chemicals! – In order to examine chemical defenses, and identify the compounds responsible, scientists often extract and separate chemical from the organism Bioassay guided fractionation – Extracted chemicals are then applied to a food and compared to the same food sans chemical

Aposematism Different strategies to avoid nasty chemicals – Blennies regurgitate treated food and then refuse to accept anything that looks like it – Killifish just learned to avoid the noxious chemical

Mimicry Batesian mimicry- a relatively scarce, palatable, and unprotected species resembles an abundant, relatively unpalatable, or well-protected species, and so becomes disguised. Batfish Advantageous when mimics are scarce relative to model Disadvantageous when mimics are abundant Although there is still lots of debate about this in the literature

Mimicry Mullerian mimicry- when two unpalatable species grow to resemble each other – Predators who learn to avoid one, learn to avoid the other The two invertebrates on the left are different species of sea slugs, while the one on the right is a marine flatworm. All three secrete noxious substances and are unpalatable.

Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage – 2) Warning Coloration – 3) Defense- toxins and other physical protection Constitutive defenses Induced defenses Don’t eat me!

Bryozoans, barnacles, and many gastropods produce spines, thickened shells, or growth asymmetries in response to waterborne predator chemical cues Induced Defenses

Marine Bryozoans Harvell 1986

Induced Defenses Chemical defenses can also be up-regulated (especially in algae)

Constitutive Defenses Less common than induced defenses in marine communities In marine environments, these are mostly chemical defense s Species or genera can differ on const. vs induced

Constitutive Defenses Why might induced defenses be more common than constitutive defenses? – Allocation costs- defenses require energy to produce – Opportunity costs- resources allocated to defenses cant be allocated elsewhere

Chemical Defenses Do chemical defenses actually reduce fitness or do they just taste bad? – Didemnins in tunicates

Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage – 2) Warning Coloration – 3) Defense- toxins and other physical protection – 4) Autotomy Don’t eat me!

Autotomy Common in crab species – Porcelain crabs in particular have a hair trigger on shedding limbs Mantis shrimp vs crab Doesnt always work....

Prey have developed multiple adaptations to avoid being eaten – 1) Camouflage – 2) Warning Coloration – 3) Defense- toxins and other physical protection – 4) Autotomy – 5) Behavioral Escape- Antipredator behaviors In space or in time! Don’t eat me!

Behavioral Escape Plankton and Small Nekton Vertical migrations – Occur in pelagic environments with no structure Forage at the surface at night and migrate to the depths during the day – More pronounced in pigmented species that are more conspicuous to visual predators (Hays et al. 1994) Migrations strength is often seasonally coordinated with predatory fish abundance

Demersal fish are thought to inhabit shallow water during the day to avoid larger fish predators and migrate to deeper depths to forage at night – But this theory has been called into question by a few studies Behavioral Escape

Predators also induce prey to seek refuges and/or reduce their activity to reduce their chance of being eaten –anti-predator behavior

Anti-predator Behaviors These antipredator behaviors also result in prey feeding reductions

Anti-predator Behaviors These antipredator behaviors also result in prey feeding reductions – Consumptive effects Or Density Mediated Interactions Changes in prey and resource abundance due to lethal interactions with predators – Non-consumptive effects Or Trait Mediated Interactions Changes in prey habitat or resource use in response to predator risk Predator Prey Resource

Non-Consumptive effects Toadfish, mud crabs, oysters Grabowski, 2004

Non-consumptive effects Toadfish, mud crabs, oysters Grabowski, 2004

Non-Consumptive Effects Spiders, grasshoppers, and grass – Consuming vs scaring

Non-consumptive Effects Which drives the majority of indirect interactions? On average, TMI’s are responsible for 85% indirect effects Preisser et al. 2005

Behavioral Escape and NCEs Behavioral escapes are often initiated once a predator has been perceived – Usually by chemical detection (although other sensory modalities are possible-they are less studied)

Behavioral Escape Experimenting with predator chemical cues

Determining prey response to cues Prey use information about cues and their environment to determine if, when, and how much they will respond Threat sensitive predator avoidance (Helfman, 1989)

What predator traits do you think affect the magnitude of anti-predator behaviors and non-consumptive effects?

Risk is context-dependent Threat sensitive predator avoidance (Helfman, 1989) – Predator Identity (Turner, 1999)

Risk is context-dependent Threat sensitive predator avoidance (Helfman, 1989) – Predator Identity (Turner, 1999)

Risk is context-dependent Threat sensitive predator avoidance (Helfman, 1989) – Predator Identity (Turner, 1999) – Predator Diet (Schoeppner and Relyea, 2005)

Diet Specific Responses The magnitude of behavioral response to diet is due to the phylogenetic relatedness of the prey (Schoeppner and Relyea, 2005)

Diet Specific Responses Predator Diet

Risk is context-dependent Threat sensitive predator avoidance (Helfman, 1989) – Predator Identity (Turner, 1999) – Predator Diet (Schoeppner and Relyea, 2005) – Predator Size (Hill and Weissburg, 2013)

NCEs and the Perception of Predator Size Examined mud crab behavior and predation on oysters in the presence of differing size caged predators Small Crab Multiple Small Crabs Large Crab 40-60mm CW >100mm CW Control Zero Crab Control 40-60mm CW

Predator Size is Perceptible in Chemical Cues Large blue crabs and multiple small blue crabs suppress mud crab foraging activity Small (non-risky) crabs do not affect foraging Predation on Oysters B N=18 ANOVA P< B A A N=18, P<0.001 Hill and Weissburg, Oecologia, 2013

Learning to run from predators How are chemical cues of predators learned?

Predation Risk Allocation Hypothesis (Lima and Bednekoff 1999) Prey behavior should depend on the duration or high risk vs. low risk situations and the level of risk associated with them Predictions – 1) As duration of predator exposure increases, prey vigilance should decrease since long periods of prey vigilance may result in an unnecessary loss in energy intake – 2) Animals exposed to lots of risk, should forage during brief safety periods, when compared to prey with infrequent risk

Predation Risk Allocation Hypothesis (Lima and Bednekoff 1999)

Prey behavior should depend on the duration or high risk vs. low risk situations and the level of risk associated with them Predictions – 3) As risk associated with high risk situations increases, prey should increase their antipredator response, but then will increase their foraging effort in low-risk situations

But the risk allocation hypothesis is a bit paradoxical – Typical dogma is that prey exposed to higher predation risk should reduce their activity and increase vigilance For instance, animals from populations with predators often have stronger responses to predation threats than prey from predator-free populations Predation Risk Allocation Hypothesis (Lima and Bednekoff 1999)

However, so far the risk allocation theory has met with mixed support – 13 studies have investigated the prediction 6 studies found no support 4 found partial support 3 fully supported model Predation Risk Allocation Hypothesis (Lima and Bednekoff 1999)