The role of prey behaviour in marine trophic cascades

Have you seen the YouTube video below, “How wolves change rivers”? This is a pretty amazing example of a trophic cascade: the affect that the top, apex predators can have on lower trophic levels, or vice versa. This example was mentioned by Professor Robert Warner from the University of California in his seminar at Macquarie University. Although Prof. Warner studies marine environments and the affects fishing can have on entire marine ecosystems, this terrestrial example emphasises the complexity of trophic cascades in both types of systems.

The human impact on marine environments is typically seen in the higher trophic levels, or the predator level3 (see diagram of trophic levels below). As Prof. Warner suggested, a trophic cascade can result from the removal of a predator from a system, which may lead to a change in the abundance of the lower trophic species1,3. However, predator loss can also influence the function of the lower trophic species, such as their behaviour3. If the behaviour of lower trophic species is changing, then what is happening to resources below this level?

Food chainSimple marine food chain with three trophic levels

 

Prey behaviour

Predators in all types of systems – freshwater, marine and terrestrial – can cause various prey responses1. For example, prey can alter their activity level and habitat use depending on whether predators are present or absent1. This is a kind of trade off1 – do they collect food or shelter from predators?

In his seminar, Prof. Warner focussed on prey feeding and movement when predators are increased or decreased in a marine ecosystem. In the presence of predators, prey use behavioural mechanisms such as avoidance and increased vigilance, leading to less feeding and changes in their diets4. Prof. Warner has found that prey weigh less in the presence of predators.

Furthermore, Madin, Gaines & Warner (2010) mention that the prey excursion distance (the distance to which the prey leave their shelter for food) can be affected by predator presence/absence. When a predator declines in a system, the prey have a kind of free range over an area, increasing their excursion rates4. The burning question is, would the system just ‘revert’ back to its pristine state when a predator is introduced back into the system?

Prey excursionPrey excursion?

Image retrieved from http://qetza.deviantart.com/art/School-of-Fish-Bus-252847804

 

The study by Madin et al. (2012), which was also discussed by Prof Warner, found this to be the case. Madin et al. (2012) compared various reefs on Line Islands and the Great Barrier Reef, with results indicating prey foraging behaviour returned to the pre-fishing state once predators recovered in the system3. This recovery actually occurred quite quickly3. Although the species studied were not representative of an entire fish ecosystem, the authors believe these results could be widespread – location wise and taxonomically3. These results could have significant implications for conservationists looking to restore marine systems to their pristine or near pristine state3.

The halo effect

It has been discussed that predators can affect the behavioural response of prey, but as Prof Warner discussed, does risk avoidance lead to changes in prey food distributions? According to Madin et al. (2012), the responses of prey to a loss of predators can cascade through the system, eventually affecting the distribution of macro-algae (primary producers)3.

In the presence of predators, herbivores will only graze in their immediate surroundings, leading to changes in distribution of algae and seagrasses – viewed as the halo effect2 (see image below). On the other hand, the absence of predators leads to a homogenous (more even) use of resources4. Hence, it may be common to assume that predator loss leads to an increase in herbivore densities, leading to a decrease in primary producers2. But is this always the case?

haloThe halo surrounding an island can vary due to prey foraging.

Image retrieved from http://www.1770reefcruises.com/

According to Prof. Warner, the predicted flow on effects can change once mesopredators are taken into account. Mesopredators are the prey that prey on smaller prey, particularly new recruits4. An increase in mesopredators will therefore see a decrease in recruits at the lower trophic levels, as well as change their behaviour4. Smaller species will avoid areas where mesopredators are present4. This then leads to an increase in the heterogeneity and abundance of macroalgae4, which can change the entire dynamics of a marine ecosystem.

Putting this into perspective

The complexity of marine ecosystems and the significance of behaviour responses is enormous. Prey behaviour is influenced by many factors – structure of habitat, food resources available, and composition of predators and grazers3. Understanding this type of complexity should have implications for current management of marine areas. This includes fishing practices as well as politically short-sighted government policies such as shark culls.

References

1. Madin, E.M., Gaines, S.D., & Warner, R.R. (2010). Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology, 91(12), 3563-3571. doi: 10.1890/09-2174.1

2. Madin, E.M., Gaines, S.D., Madin, J.S., & Warner, R.R. (2010). Fishing indirectly structures macroalgal assemblages by altering herbivore behavior. The American Naturalist, 176(6), 785-801. doi: 10.1086/657039

3. Madin, E.M., Gaines, S.D., Madin, J.S., Link, A.K., Lubchenco, P.J., Selden, R.L., & Warner, R.R. (2012). Do behavioral foraging responses of prey to predators function similarly in restored and pristine foodwebs?. PloS one, 7(3), 1-9. doi: 10.1371/journal.pone.0032390

4. Warner, R. (2014, March 19). Fear and longing: Predator change and the role of behaviour in marine conservation. BioSeminar. Conducted from Macquarie University, North Ryde, NSW.

Sociality in an Australian huntsman spider: Delena cancerides

With over 44,000 spider species in the world2, how do you pinpoint one species to study? Dr Lynda Rayor, from Cornell University, has done just that, presenting a seminar at Macquarie University on one very unusual spider species – Delena cancerides.

D. cancerides is an Australian huntsman spider within the family Sparassidae3 that exhibits a prolonged sub-social behaviour2. This is quite peculiar considering that, according to Dr Rayor, sociality is rare in spiders other than initial maternal care of egg sacs. Furthermore, the majority of spiders that are social spin webs, which allows the spiders to cooperate on prey capture and reduce their silk costs. However, D. cancerides also exhibits this trait of a tightly associated, long lasting colony, with one very big difference – it does not build webs3.

Image Photo of D. cancerides – an adult female and offspring. Source:  Agnarsson, I., & Rayor, L. S. (2013, p. 896).

The miniature commune

Dr Rayor has observed colonies of 20 to 200 individuals living in a retreat under the bark of Eucalypts, Casuarinas or dead Acacias.  The retreat comprises of a matriarch and her offspring of various cohorts (or ages)3 (see image below). Dr Rayor’s research has shown that individuals will disperse from the colony only once they are sexually mature (approximately 1 year old).

Image

Instars – the different age groups of D. cancerides in the colony. Source: Yip, E. C., & Rayor, L. S. (2013, p. 1162).

The edges of the retreat are sealed with silk at the top and bottom, which according to Dr Rayor, is large enough for the adult female to guard the entrance. This could possibly be a mechanism of protecting the colony and keeping watch, making it hard for predators to access the retreat3.

Next of kin?

Yip et al. (as cited in Yip & Rayor, 2011) determined through allozyme analyses (a type of genetic analysis) of D. cancerides colonies, that most of the offspring were either full or half siblings. Interestingly though, there were actually unrelated spiders in up to half of the colonies studied. Dr Rayor explains that this is possible because spiders can get lost when foraging at night – they go home to the wrong colony! Individuals of less than 6 instars have a greater possibility of being integrated into the new colony. Older spiders are usually seen as a threat and shooed away, or killed.

Image D. cancerides appearing from under the bark of a tree. Source: Yip, E. C., & Rayor, L. S. (2011, p. 1938)

The sibling conundrum

The study by Yip & Rayor (2013) found that younger D. cancerides of 4th to 5th instar were heavier when their older siblings were present – an indication that younger siblings can benefit from the presence of their older siblings.

Dr Rayor has observed older siblings sharing prey with up to 22 of their younger siblings. She states that although this only occurs 5% of the time (which may not seem like much), it is actually quite significant considering this is not a very common occurrence in spider species. Dr Rayor explains that it is less energy intensive if older spiders share their prey than to continually protect it from younger siblings.

However, it may not all be about prey sharing. Yip & Rayor (2013) explain that the heavier weights could be a result of younger siblings scavenging the prey scraps from the older siblings – not prey sharing. This process can also be referred to as a producer-scrounger system, and may be similar to what has been described within the literature as ‘tolerated theft’ by primates.

Such leisurely dispersal

Why does D. cancerides remain in colonies until they are sexually mature before they disperse? There are two major reasons: cost and habitat saturation3.

#1: The very little cost

  • There is no major food competition within the colony, even if the older spiders have to share some prey with their younger siblings3.
  • Offspring can benefit from their mum – she’s very efficient at eliminating predators with her aggressive attitude. This is particularly handy for the youngsters that cannot defend themselves very well3.
  • Individual tolerance to each other (or lack of cannibalism). Dr Rayor’s new research suggests that the lower metabolic rate of D. cancerides means they can survive on low prey availability, leading to a low cannibalism rate amongst this species.

#2: Habitat saturation

There is no spare space for spiders to disperse – retreats are usually 100% occupied. A small spider would find it extremely difficult to secure a retreat that wasn’t occupied. Therefore, waiting until they are larger and more able to defend themselves is a useful tactic3.

Food (or spiders) for thought

With increasing habitat fragmentation and destruction leading to further habitat saturation, could D. cancerides develop a more relaxed strategy to the kids staying at home? Furthermore, Dr Rayor found that as habitat saturation increases, the occupants become larger, as they are best at competing for new resources (survival of the fittest). Does this mean that, in an evolutionary sense, D. cancerides may become a larger species in the future?

References

1 Agnarsson, I., & Rayor, L. S. (2013). A molecular phylogeny of the Australian huntsman spiders (Sparassidae, Deleninae): Implications for taxonomy and social behaviour. Molecular phylogenetics and evolution, 69(3), 895-905. doi: 10.1016/j.ympev.2013.06.015

2 Rayor, L. (2014, March 5). Adaptations for living with cannibals: Evolution of sociality in Australian huntsman spiders. BioSeminar. Conducted from Macquarie University, North Ryde, NSW.

3 Yip, E. C., & Rayor, L. S. (2011). Do social spiders cooperate in predator defense and foraging without a web?. Behavioral Ecology and Sociobiology, 65(10), 1935-1947. doi: 10.1007/s00265-011-1203-5

4 Yip, E. C., & Rayor, L. S. (2013). The influence of siblings on body condition in a social spider: is prey sharing cooperation or competition?. Animal Behaviour, 85(6), 1161-1168. doi: 10.1016/j.anbehav.2013.03.016