It’s well known that removing large numbers of top predators from the ocean impacts on the abundance of their prey, their prey’s prey and the small creatures and vegetation those prey eat: a phenomenon called a ‘trophic cascade’.

However, according to Professor Robert Warner of the University of California Santa Barbara, it’s not just a simple numbers game. By removing the top predators, we are also indirectly affecting the behaviour, reproduction and diet of prey and predator alike, changes that are potentially more disruptive for marine ecosystems than simple predation alone [1]. Professor Warner is in Australia as the 2013 recipient of the prestigious Selby travelling award and is discussing some of these indirect effects at Macquarie University today.

Parrotfish hiding from predators (photo: Peter Vorotnikov)

Parrotfish hiding from predators (photo: Peter Vorotnikov)

Changes to risk avoidance behaviour in prey – No longer ‘damsels in distress’

Prey species are not inert objects that hang around wearing signs saying ‘eat me!’ Quite sensibly, they avoid being eaten by lurking in shelters and darting around skittishly, one eye always scanning for predators while the other is searching around for a good patch of seagrass to eat. Traits such as vigilance and risk avoidance have been selected for over many generations: After all, slow pokes and day dreamers get picked off by predators and therefore don’t get to leave their genetic mark on the next generation [2].

In coral reef environments, Warner explains, fear of predators compels small prey species, such as damselfish, to stay close to shelter, grazing almost exclusively at their own back door [2, 3]. This leads to an uneven distribution of seagrasses throughout the environment: overgrazed patches radiate out from the shelters, creating a halo pattern which Warner refers to as a ‘landscape of fear’. A pattern that is apparently visible from space [4].

A. Halos visible in Heron Island, the Great Barrier Reef Australia B. No halos visible in the heavily fished Panggang Island in Indonesia's Thousand Islands (Kepulauan Seribu) (Madin et al., 2011)

A. Halos visible in Heron Island, the Great Barrier Reef Australia B. No halos visible in the heavily fished Panggang Island in Indonesia’s Thousand Islands (Kepulauan Seribu) (Madin et al., 2011)

However, when human fishing eliminates large predators from an environment, the resident prey are suddenly free to venture further from their shelters in order to find optimal food sources [3, 5]. While a better diet enables them to grow heavier and more robust than neighbours from high-predator environs [2, 6], a larger excursion range leads to more evenly distributed algae grazing [2, 5]. This can have an impact on reef health, as algae compete with coral species for reef space [2].

These discoveries are important, insists Warner, because they illustrate how human fishing can initiate behaviour change across a whole population not just in individuals [3].

Changes to predator population structure – Where have all the good men gone?

A glance at historical ‘trophy fish’ catch photographs show how fish populations are shrinking, not only in number but in specimen size [7]. This is because both commercial and game fishing target the largest fish. After all, every fisherman wants his ‘triumphant catch’ story.

Historical trophy fish catch photographs from the Florida Keys, USA, showing general decrease in size of individual specimens. A. 1957 B. 1980s C. 2007 (McClenachan, 2009)

Historical trophy fish catch photographs from the Florida Keys, USA, showing general decrease in size of individual specimens. A. 1957 B. 1980s C. 2007 (McClenachan, 2009)

And herein lays the problem, explains Warner. By targeting large fish, we are targeting males, and thus inadvertently altering the overall gender structure of predator populations. This is particularly significant in gender-bending species.

In some of these species, gender-switching is mediated by social cues: In overfished areas, females switch gender at a much smaller size than usual to compensate for the lack of males [8, 9].  But these are the lucky ones, says Warner. Species with age or size-mediated gender switching can’t change sex at will. An ensuing ‘man drought’ leads to large swathes of eggs being released unfertilised [8, 9].

But the smaller average fish size not only has a devastating effect on fertility, it also has an effect on diet. This is because smaller fish don’t swim as fast as their larger compatriots, and have smaller jaws. Both features lead to dietary alterations, which can have knock-on effects for the whole reef ecosystem. Warner cites the example of California sheepshead, whose lower average size has impeded their ability to consume their usual diet, leading to a proliferation of kelp-munching sea-urchins [9].fish pic2

The effects of reserves on recovery of fish behaviour – is it all doom and gloom?

So can ecosystems recover from the indirect effects of human fishing? Evidence offered by Warner suggests that they can, and that in fact, behaviour recovery occurs quicker than numerical recovery [5].

Firstly, Warner tells us, within five years of reserve creation in the Line Islands, damselfish and parrotfish have recovered risk avoidance behaviour [5]. Secondly, within one generation after a reserve was created in California, Sheepshead sex-change timing recovered to close to pre-predation sizes, as did their dietary control of sea urchin populations [9]. These examples show the enormous plasticity of fish behaviour and life history events [5].

Whichever way you look at it, concludes Warner, the evidence is clear. When designing marine conservation management strategies, it is imperative to consider the indirect effects of human fishing from the population level to the whole marine ecosystem.


1.Preisser, E.L., D.I. Bolnick, and M.F. Benard, Scared to death? The effects of intimidation and consumption in predator-prey interactions. Ecology, 2005. 86(2): p. 501-509.
2.Madin, E.M.P., et al., Fishing Indirectly Structures Macroalgal Assemblages by Altering Herbivore Behavior. American Naturalist, 2010. 176(6): p. 785-801.
3.Madin, E.M.P., S.D. Gaines, and R.R. Warner, Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology, 2010. 91(12): p. 3563-3571.
4.Madin, E.M.P., J.S. Madin, and D.J. Booth, Landscape of fear visible from space. Scientific Reports, 2011. 1(14).
5.Madin, E.M.P., et al., Do Behavioral Foraging Responses of Prey to Predators Function Similarly in Restored and Pristine Foodwebs? Plos One, 2012. 7(3).
6.Walsh, S.M., et al., Fishing top predators indirectly affects condition and reproduction in a reef-fish community. Journal of Fish Biology, 2012. 80(3): p. 519-537.
7.McClenachan, L., Documenting Loss of Trophy FIsh from the Florida Keys with Historical Photographs. Conservation Biology, 2009. 23: p. 636-643.
8.Hamilton, S.L., et al., Size-selective harvesting alters life histories of a temperate sex-changing fish. Ecological Applications, 2007. 17(8): p. 2268-2280.
9.Hamilton, S.L., S.D. Newsome, and J.E. Caselle, Dietary niche expansion of a kelp forest predator recovering from intense commercial exploitation. Ecology, 2014. 95(1): p. 164-172.
10.DeMartini, E.E., A.M. Friedlander, and S.R. Holzwarth, Size at sex change in protogynous labroids, prey body size distributions, and apex predator densities at NW Hawaiian atolls. Marine Ecology Progress Series, 2005. 297: p. 259-271.


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