0 views

Uploaded by Aurivas

Art

- ACSA.AM.86.3
- Extreme climatic events.pdf
- askdjfhasl.pdf
- Lipschitz Condition
- Jane Lubchenco
- Script PDE
- ch1
- Persistence Tutorial
- Autonomous Equations
- Inter Specific Competition
- A.new.Class.molecules2006.E
- MMChapter6_6p3
- 2009 April Malang East Java the Jakarta Globe Students Get Practical Lessons in Ecological Responsibility_1
- predator-prey populations report
- A 03401001005
- Math 10
- 1. DEFINISI EKOLOGI
- programmetables12_0
- ecosystems
- Hudson River Sustainable Shorlines Project Overview

You are on page 1of 11

Role reversal in a

rsos.royalsocietypublishing.org

predator–prey interaction

Faustino Sánchez-Garduño1 , Pedro Miramontes1,2 and

Tatiana T. Marquez-Lago3

Research 1 Facultad de Ciencias, Universidad Nacional Autónoma de México, México DF., 04510,

Mexico

Cite this article: Sánchez-Garduño F, 2 Centro de Ciencias de la Complejidad, Universidad Nacional Autónoma de México,

Miramontes P, Marquez-Lago TT. 2014 Role

México DF., 04510, Mexico

reversal in a predator–prey interaction. R. Soc. 3 Integrative Systems Biology Unit, Okinawa Institute of Science and Technology,

open sci. 1: 140186. Onna-son, Okinawa 904-0412, Japan

http://dx.doi.org/10.1098/rsos.140186

1. Summary

Predator–prey relationships are one of the most studied

Received: 18 June 2014

interactions in population ecology. However, little attention has

Accepted: 27 August 2014 been paid to the possibility of role exchange between species,

despite ﬁrm ﬁeld evidence of such phenomena in nature. In this

paper, we build a mathematical model capable of reproducing

the main phenomenological features of role reversal in a classical

Subject Areas: system and present results for both the temporal and spatio-

temporal cases. We show that, depending on the choice of

computational biology/ecology/

parameters, our role-reversal dynamical system exhibits excitable-

mathematical modelling like behaviour, generating waves of species’ concentrations that

propagate through space. Our ﬁndings ﬁll a long-standing gap

Keywords: in modelling ecological interactions and can be applicable to

predator–prey, bistability, excitable media, better understanding ecological niche shifts and planning of

reaction–diffusion sustainable ecosystems.

Tatiana T. Marquez-Lago Predator–prey interactions have been widely studied in the last

e-mail: tatiana.marquez@oist.jp hundred years, and their mathematical models are among the

oldest established in ecology. One of the classic ecological models,

the Lotka–Volterra model, was independently proposed by Alfred

J. Lotka and Vito Volterra in the ﬁrst quarter of the 1900s.

Alfred J. Lotka developed preliminary models with a focus

on demography, but later reﬁned his model while turning his

attention to trophic interactions by using a plant species and a

herbivorous animal as an example. Vito Volterra, on the other

hand, is said to have developed his version of the model by

analysing ﬁshery patterns in the Adriatic Sea. The wide origins

and scales of the questions that led to this classic model show

its inherent ﬂexibility and adaptability, a probable reason why

Lotka–Volterra models remain popular to this day.

Electronic supplementary material is available Over the years, many modiﬁcations have been made to the

at http://dx.doi.org/10.1098/rsos.140186 or via original Lotka–Volterra model, to adapt to more realistic physical

http://rsos.royalsocietypublishing.org.

2014 The Authors. Published by the Royal Society under the terms of the Creative Commons

Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted

use, provided the original author and source are credited.

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

scenarios. Some examples are competition, mutualism [1] and generalization to several interacting

2

species. However, so far, little has been done in generating models where the role of interacting species

can change in time. Models of this sort are essential, as the ecological role of individual species may not

.................................................

be ﬁxed, nor clear [2].

Role-exchanges, or role-reversals, are actually more common in nature than once believed. For

instance, prey species may confront predators in a size-dominant manner [3–6], size-recessive manner

[7], by changing population densities [8], or without speciﬁc trophic intentions [9]. Also, it is known

that adult prey of some species attack vulnerable young predators, where prey recognize the species of

predators they were exposed to during juvenile stages, and effectively attack their offspring [2,10].

So, the goal of our work was to ﬁll this gap and propose a model that could account for role-reversal

interactions. For that purpose, we focused on representing one of the classic references in the literature,

the work by Barkai and McQuaid. However, it is important to note that the deﬁnition of interaction

(trophic, sexual and hierarchical) can be easily modiﬁed once a model is constructed and, thus, our work

is not solely limited to interactions of one type.

In 1988, Barkai & McQuaid [8] reported a novel observation in population ecology while studying

benthic fauna in South African shores: a predator–prey role reversal between a decapod crustacean and

a marine snail. Speciﬁcally, in Malgas Island, the rock lobster Jasus lalandii preys on a type of whelk,

Burnupena papyracea. So, as could be easily expected, the population density of whelks soared upon

lobsters’ extinction in a nearby island (Marcus Island, just 4 km away from Malgas). However, in a series

of very interesting controlled ecological experiments, Barkai and McQuaid reintroduced a number of

J. lalandii in Marcus Island to investigate whether the equilibrium observed in the neighbouring Malgas

Island could be restored. The results were simply astounding:

‘The result was immediate. The apparently healthy rock lobsters were quickly overwhelmed by

large number of whelks. Several hundreds were observed being attacked immediately after release

and a week later no live rock lobsters could be found at Marcus Island.’ [8, p. 63]

Surprisingly, and despite observations such as the report in [8], theoretical population biology has

largely ignored the possibility of predators and preys switching their roles. Of importance, the paper of

Barkai and McQuaid suggests the existence of a threshold control parameter responsible for switching

the dynamics between (i) a classical predator–prey system with sustained or decaying oscillations, and

(ii) a predator (the former prey) driving its present-day prey to local extinction.

In this paper, we build a model capable of reproducing this behaviour. It is worth noting that there

are some papers in the literature describing ratio-dependent predation (e.g. [11,12]), but they are not

related to the possibility of role-reversals. On the other hand, the likelihood of changing ecological

roles as a result of density dependence has already been documented for the case of mutualism by

Breton & Addicott [13] and, in 1998, Hernández and Barradas made an interesting effort to build a

mathematical scheme capable of taking into account the possible switches among different possible

ecological interactions [14]. So, to the best of our knowledge, this is the ﬁrst theoretical study—supported

by ﬁeld evidence—speciﬁcally addressing predator–prey role-reversals.

3. Mathematical model

Predator–prey systems are generally modelled by adopting one of the many variations of the classical

Lotka–Volterra model:

ẋ = αx − βxy

(3.1)

and ẏ = −γ y + δxy,

where α denotes the intrinsic preys’ rate of growth, β corresponds to the rate of predation upon prey, γ

stands for the predators’ death rate in the absence of prey and δ represents the beneﬁt of predators due to

the encounters with prey. Our goal is to assess whether modelling the role-reversal behaviour observed

by Barkai & McQuaid [8] is possible, when adopting appropriate parameters and assumptions.

For instance, if one considers quadratic density dependence in the prey as well as in the predators,

non-constant rates of consumption of prey by the predators, and the proﬁting of predators by the

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

3

⎫

A

ẋ = Bx − x − C(x)xy⎪⎬

.................................................

B (3.2)

⎪

⎭

and ẏ = −Dy − Ey2 + F(x)xy,

where B represents the intrinsic growth rate of the prey in the absence of predators, A/B the carrying

capacity of the prey’s habitat, C(x) the rate of prey consumption by the population of predators, D the

predators’ decay rate in the absence of prey, E the intraspeciﬁc rate of competition among predators and,

ﬁnally, F(x) the factor of predator’s proﬁting from prey. The ratio F(x)/C(x) is then the fraction of prey

biomass that is actually converted into predator biomass. The latter should remain constant, because the

fraction of preys’ biomass converted to predators’ biomass is a physiological parameter, rather than a

magnitude depending on demographical variables.

A particular case of system (3.2) in appropriate rescaled variables can be written as:

ẋ = bx(1 − x) − cx(k − x)y ≡ f (x, y)

(3.3)

and ẏ = −ey(1 + y) + fx(k − x)y ≡ g(x, y),

where all the parameters are positive and 0 < k < 1. In fact, all of the parameters have a relevant ecological

interpretation: b is the normalized intrinsic growth rate of the species with density x, c is a measure of

the damage intensity of the second species on the ﬁrst one, e is the normalized rate of predators decay

and f is the beneﬁt (damage) the second population gets from the ﬁrst one. Note the crucial role played

by the interaction term x(k − x), where k stands for the ﬁrst population threshold to switch from being

prey to predator.

4.1. Nullclines and equilibria

After some basic algebra, it can be noted that the horizontal nullcline of the system of equations (3.3),

that is [b(1 − x) − c(k − x)y]x = 0, has two branches: the vertical axis and the non-trivial branch

b(1 − x)

yh (x) = , (4.1)

c(k − x)

which is a symmetric hyperbola with asymptotes: x ≡ k and y = b/c (ﬁgure 1). The vertical nullcline,

[−e(1 + y) + fx(k − x)]y = 0, also has two branches: the horizontal axis and the non-trivial branch

fx(k − x)

yv (x) = − 1, (4.2)

e

which is a parabola with yv (0) = yv (k) = −1, attaining its maximum at x = k/2, the value of which is

k fk2

yv = − 1.

2 4e

This term is positive if and only if fk2 > 4e. The zeros, x1 and x2 , of equation (4.2) are given by

f ± f 2 k2 − 4fe

x1 , x2 = .

2f

The latter are real numbers if and only if fk2 ≥ 4e. The rate of change of yv is then

f

yv (x) = (k − 2x).

e

To analyse the system while keeping in mind the ecological interpretation of the variables and

parameters, we will now consider the left branch of the horizontal nullcline (4.1), fk2 > 4e with 0 < k < 1

and the region of the phase plane of the system of equations (3.3) deﬁned as

The system of equations (3.3) has the equilibria: P0 = (0, 0), P1 = (1, 0) plus those states of the system

stemming from the intersection of the nullclines yh and yv in the region R. Such equilibria are deﬁned

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

8 4

6

.................................................

y4

P3

2 P2

P1

0 0.2 0.4 0.6 0.8 1.0 1.2

x

Figure 1. Nullclines of the system of equations (3.3). The continuous downward facing parabola and the horizontal axis are the vertical

nullcline. All other lines, dotted and the vertical axis are the horizontal nullcline. P1 , P2 and P3 are the non-trivial equilibria. The origin of

coordinates is a trivial equilibrium.

b(1 − x) fx(k − x)

= − 1, (4.3)

c(k − x) e

or, equivalently, the x that are roots of the third-order polynomial

The calculation of the non-trivial equilibria of equation (3.3) follows from the determination of the

roots of equation (4.4). Consequently, owing to the qualitative behaviour of the functions yh and yv on

R, we are faced with the following possibilities.

1. The non-trivial branches of the nullclines do not intersect each other in the region of interest. In

such a case, the system (3.3) has just two equilibria: P0 and P1 in R. Figure 2a shows the relative

position of the nullclines in this case, and ﬁgure 3a the phase portrait of the system. For ﬁxed

positive values of b, c, e and f , and k ∈ (0, 1) such that (fk2 /4e) > 1 one can see that both nullclines

become closer with increasing values of k.

2. The nullclines yh and yv touch each other tangentially at the point P∗ = (x∗ , y∗ ) in the region R.

Again, ﬁgure 2b shows the relative position of the nullclines in this case, and ﬁgure 3b the phase

portrait of the system. In such a case x∗ , in addition to satisfy equation (4.3), must also satisfy the

condition yh (x) = yv (x), i.e.

b (1 − k) f

= (k − 2x). (4.5)

c (k − x) 2 e

If one assumes the existence of x∗ satisfying equation (4.3), the required extra condition (4.5)

imposes the restriction 0 < x∗ < k/2 on x∗ , owing to the positiveness of its left-hand side.

Moreover, from a geometrical interpretation of equation (4.5), it follows that, if:

—

fk b (1 − k)

< ,

e c k2

there is not any x ≥ 0 such that yh (x) = yv (x).

—

fk b (1 − k)

= ,

e c k2

the condition (4.5) is satisﬁed just at x = 0.

—

fk b (1 − k)

> ,

e c k2

there exists exactly one value, x∗ ∈ (0, k/2), of x > 0 such that the equality (4.5) holds.

In any case, the point P∗ is a non-hyperbolic equilibrium of the system of equations (3.3). In fact,

the proof that a tangential contact of the nullclines results in a point where the determinant of

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

(a) (b)

8 8 5

7 7

.................................................

6 6

5 5

y 4 y 4

3 3

2 2

1 1

0 0.2 0.4 0.6 0.8 1.0 1.2 0 0.2 0.4 0.6 0.8 1.0 1.2

x x

Figure 2. The relative position of the nullclines can be parametrically controlled. In (a), the downward facing parabola does not intersect

the upper branch of the hyperbola. After a small change in the parameter k, both nullclines touch tangentially, as in (b). Further changes

in the parameter lead to a saddle-node bifurcation and to the two transversal intersections depicted in figure 1.

(a) (b)

8 8

7 7

6 6

5 5

y 4 y 4

3 3

2 2

1 1

0 0.2 0.4 0.6 0.8 1.0 1.2 0 0.2 0.4 0.6 0.8 1.0 1.2

x x

Figure 3. Phase portrait of the system. Blue/dark lines correspond to trajectories, whereas grey/light lines correspond to nullclines. When

nullclines do not intersect, as seen in case (a), the origin is a saddle and there is only a non-trivial equilibrium on the x-axis, which is stable.

All the initial conditions lead to lobsters extinction. However, when there is a tangential contact between the nullclines, as in case (b),

there is a new non-hyperbolic equilibrium point, which is a saddle node.

the Jacobian matrix of the system vanishes follows immediately, implying that at least one of its

eigenvalues is zero.

3. The nullclines intersect each other transversally at two points, P2 and P3 , belonging to the region

R. For reference, please refer to ﬁgure 1. In this case, the system of equations (3.3) has two extra

equilibria which arise from the bifurcation of P∗ . Here, if in addition to choosing the parameters

f , k and e such that fk2 /4e > 1, we select the rest of them such that:

fk2 b

− 1 > (2 − k),

4e c

guaranteeing the existence of the equilibria P2 = (x̃2 , ỹ2 ) and P3 = (x̃3 , ỹ3 ) mentioned above.

Moreover, the coordinates of these points satisfy 0 < x̃2 < k/2, k/2 < x̃3 < k, ỹi > 0 with ỹ2 <

ỹ3 . Here, i = 2, 3.

— yh (k/2) = yv (k/2), i.e.

fk2 b

− 1 = (2 − k).

4e c

Here, we have P2 = (x̃2 , ỹ2 ) with 0 < x̃2 < k/2 and 0 < ỹ2 < (b/c)(2 − k). Meanwhile, P3 =

(k/2, (b/c)(2 − k)).

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

8 6

7

.................................................

6

5

y4 P3

P2

3

2

1 P1

x

Figure 4. The equilibria of system (3.3). P1 and P2 are stable, whereas P3 is a saddle point. It is worth noting P1 is a node and P2 could

be a node or a focus, depending on the parameter values. The heteroclinic trajectory joining the saddle point to the stable node is easily

identified. The stable manifold is a separatrix between the basin of attraction of P1 and P2 . The following parameters were used: k = 0.8,

b = 0.6, c = 0.3, e = 0.05 and f = 2.

Part of the local analysis of the system of equations (3.3) is based on the linear approximation around its

equilibria. Thus, we calculate the Jacobian matrix of the system (3.3):

b(1 − 2x) − cy(k − 2x) −cx(k − x)

J[f1 , f2 ](x,y) = . (4.6)

fy(k − 2x) −e − 2ey + fx(k − x)

By a straightforward calculation, we obtain the eigenvalues of the Jacobian matrix (4.6) at the point

P0 . These are: λ1 = b > 0 and λ2 = −e < 0. Hence, P0 is saddle point of the system (3.3), for all positive

parameter values. By carrying out similar calculations, we obtain the corresponding eigenvalues of

matrix (4.6) at P1 , which are: λ1 = −b < 0 and λ2 = f (k − 1) − e. The restriction 0 < k < 1 on k implies that

(f (k − 1) − e) < 0. Therefore, P1 is an asymptotically stable node for all the positive parameter values

appearing in system (3.3).

Now we carry out the local analysis of (3.3). We note two cases, depending on the relative position of

the nullclines.

Case 1. The main branches (4.1) and (4.2) of the nullclines do not intersect on R. Here, any trajectory

of system (3.3) starting at the initial condition (x0 , y0 ) with positive x0 and y0 tends to the equilibria

P1 as time goes to inﬁnity. Thus, the region R+ is the basin of attraction of P1 . Invariably, the species

with density y vanishes, implying non-coexistence among the interacting species. Meanwhile, the other

species approach the associated carrying capacity.

Case 2. The nullclines intersect each other at the points P2 = (x̃2 , ỹ2 ) and P3 = (x̃3 , ỹ3 ), where none is

tangential. Here, x̃2 and x̃3 satisfy 0 < x̃2 < k/2 and k/2 < x̃3 < k. In a neighbourhood of P2 and P3 , the

functions f1 and f2 satisfy the implicit function theorem. In particular, each one of the identities f1 (x, y) = 0

and f2 (x, y) = 0 deﬁne a function there. Actually, these are yh (x) and yv (x) given in equations (4.1) and

(4.2), respectively. Their respective derivative at x̃i with i = 2, 3 is calculated as follows:

f1x (x̃i , ỹi ) f2x (x̃i , ỹi )

yh (x̃i ) = − and yv (x̃i ) = − .

f1y (x̃i , ỹi ) f2y (x̃i , ỹi )

By using these equalities, we can state the following proposition.

Proposition 4.1. The equilibrium P2 is not a saddle point. Meanwhile, the equilibrium P3 is a saddle point for

all the parameter values.

A proof of this proposition and some remarks can be found in the electronic supplementary material,

Appendix A.

As we have already shown, the system (3.3) could have up to four equilibrium points. These are

illustrated in ﬁgure 4. The origin of coordinates is a saddle point with the horizontal and vertical axis

as its unstable and stable manifolds. P1 and P3 are, respectively, a node and a saddle for parameter

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

values after the bifurcation, and P2 could be a stable node. The stable manifold of the saddle point is

7

a separatrix dividing the phase space in two disjoint regions: the set of initial conditions going to P1 ,

and the complement with points going to P2 . Moreover, our numerical solution shows the existence of a

.................................................

homoclinic trajectory starting and ending in the saddle point. Thus, we have a bistable system.

The bistability of system (3.3) has an interesting ecological interpretation: the coexistence of the

interacting species occurs whenever the initial population densities (x0 , y0 ) are located in the region

above the saddle point unstable manifold. In this case, both populations evolve towards the attractor

P2 . On the other hand, if the initial population densities (x0 , y0 ) are below the separatrix, the population

densities (x(t), y(t)) evolve towards the equilibria P1 , implying the non-coexistence of the species and,

invariably, the species with population density y vanishes. The heteroclinic trajectory of system (3.3)

connecting the saddle (P3 ) with the node (P2 —or focus, depending on the set of parameters), in addition

to the coexistence of the species, also tells us that this occurs by the transition from one equilibrium to

another as time increases.

5. Spatial dynamics

To describe more accurately our role-reversal system, we extended our model of system (3.3) to

incorporate the spatial variation of the population densities and conﬁrm that our ﬁndings hold in spatial-

explicit scenarios. Here, if we denote by u(r, t) and v(r, t), the population density of the whelks and

lobsters at the point r at time t, the resulting model is

⎫

ut = Du ∇ 2 u + bu(1 − u) − cu(k − u)v ⎬

(5.1)

and vt = Dv ∇ 2 v − ev(1 + v) + fu(k − u)v, ⎭

where the subscript in u and v denotes the partial derivative with respect to time, and ∇ 2 is the laplacian

operator. Here, Du > 0, Dv > 0 correspond to the diffusivity of the species with density u and v, i.e. that

of whelks and lobsters, respectively. It is worth noting that the original variables have been rescaled, but

still denote population densities.

We then proceeded to construct numerical solutions of the system (5.1) in three different domains: a

circle with radius 2.2 length units (LU), an annulus deﬁned by concentric circles of radii 2.2 and 1 LU, and

a square with side length of 4.6 LU. All domains were constructed to depict similar distances between

Malgas Island and Marcus Island (roughly 4 km). In the ﬁrst one, the annular domain, we try to mimic

the island habitat of whelks and lobsters as a concentric domain. The other two domains are used to

conﬁrm the pattern formation characteristic of excitable media and to reject any biases from the shape of

the boundaries.

To obtain numerical solutions of all spatial cases, we used the ﬁnite-element method with adaptive

time stepping and assumed zero-ﬂux boundary conditions. Accordingly, we discretized all spatial

domains by means of Delaunay triangulations, until a maximal side length of 0.17 LU was obtained. The

latter deﬁnes the approximation error of the numerical scheme. We attempted to describe two entirely

different situations by using a single set of kinetic parameters: that of Malgas Island, where both species

coexist, and Marcus Island, where whelks soar and lobsters become extinct. The only difference between

these two cases was the initial conditions used.

In terms of parameters, while there is no data speciﬁc to J. lalandii and B. papyracea in islands of the

Saldanha Bay, data of similar species can be found in the literature. For instance, a related rock-lobster

species, Jasus Edwardii has been found to move at a rate of 5–7 km d−1 [15]. By contrast, whelks within

the superfamily Buccinoidea have been found to move towards food at rates between 50 and 220 m d−1

[16,17]. Importantly, predation by whelks remains seemingly unaffected by variations in water ﬂow. In

more detail, the statistical analysis in [18] showed no detectable differences between the total distances

moved by whelks in reduced and enhanced ﬂows. Moreover, whelk burrowing, prey searching and

overall movement patterns were observed to be similar in both ﬂow regimes. The likely reason for this

is that whelks are slow moving, predatory gastropods that often forage with their bodies buried in the

sediment and, among many key factors, they are less susceptible to ﬂow-induced distortion of prey

odour plumes. Of importance, the ranges of ﬂow included in [18] were vast, matching conditions typical

of benthic ﬂows.

By putting these ﬁndings together, we argue a reasonable model need not incorporate inﬂuences

from shallow water currents and would assume whelks to move towards ‘bait’ at a speed roughly

one order of magnitude smaller than that of lobsters. Thus, we opted for a two-dimensional habitat,

and one order of magnitude difference between the non-dimensional isotropic diffusion rates (Du = 0.01

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

(a) (b)

8

0.06

1.0

.................................................

whelk density

0.04

0.5 annulus

0.02 circle

rectangle

0 0

(c) (d)

0.45

0.10

annulus

lobster density

circle

0.35 rectangle

0.05

0.25

0 2 4 6 8 10 0 2 4 6 8 10

time time

Figure 5. Time evolution of whelk and lobster densities, in different spatial domains. Cases (a,c) correspond to initial conditions

representing Malgas Island, whereas (b,d) correspond to initial conditions representing Marcus Island.

and Dv = 0.1). Aside, our choice of reaction parameters was: b = 10, c = 33.8, e = 0.5, f = 30 and k = 0.9.

Regarding initial conditions, we adopted the following scenarios, representing the different scenarios of

weighted biomass.

1. Malgas Island: the initial density of whelks u at each element was drawn from a uniform

distribution 0.1 ∗ U(0.2,0.3), and that of lobsters v from U(0.2,0.3).

2. Marcus Island: the initial density of whelks u at each element was drawn from a uniform

distribution U(0.2,0.3), and that of lobsters v from 0.1 ∗ U(0.2,0.3).

The choice of reaction parameters was made upon a quick parameter sweep, leading to excitable-

like behaviour. However, it should be noted many sets of parameters can be compatible with a given

population dynamic. Regarding initial conditions, spatial simulations were performed with random

initial conditions. In this way, it is possible to denote emergent patterns as robust with respect to variable

initial conditions, and entirely independent of any pre-pattern. Numerical solutions of system (5.1) are

shown in ﬁgure 5, corresponding to averaged densities of whelks and lobsters in the three different

spatial domains, respectively. Movies of the corresponding simulations in an annular domain can also be

found in the electronic supplementary material.

Interestingly, changes in density are usually accompanied with wave-like spatial transitions in each

species density. Examples of such spatial transient patterns can be found in ﬁgures 6 and 7, for annular

and rectangular domains in Malgas Island and Marcus Island, respectively.

We have modelled a well-documented case of role-reversal in a predator–prey interaction, capturing the

essential ecological factors within the study of Barkai & McQuaid [8], who did extraordinary ﬁeldwork

and meticulously reported this striking role-reversal phenomenon happening between whelks and

lobsters in the Saldanha Bay.

The analysis of our model and corresponding numerical solutions clearly predict the coexistence

of both populations and the switching of roles between the once denoted predators and prey. Here,

the coexistence scenario corresponds to the case when lobsters predate upon whelks, and role-reversal

corresponds to the case when whelks drive the population of lobsters to extinction, as observed by

Barkai & McQuaid [8] in the ﬁeld. However, it should be noted that in our model the switching of roles

can occur for inﬁnitely many combinations of the parameters. Speciﬁcally, the switching will occur when

a state of the system crosses the separatrix, the unstable manifold of the saddle point in ﬁgure 4.

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

2.0

9

2.0 0.028

0.028

1.5

1.5

.................................................

0.027

0.027 1.0

1.0

0.026

0

0

0.025 0.025

–0.5

–0.5

–1.0

0.024 –1.0 0.024

–1.5

–1.5

–2.0 0.023 0.023

–2.0

–2.5

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.022 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 0.022

0.0105 0.0109

2.5 3.0

0.0108

1.5

1.0 0.0103

0.0107

1.0

0.5 0.0102

0.5 0.0106

0 0.0101

0

0.0105

–0.5 0.0100 –0.5

0.0104

–1.0 0.0099 –1.0

–1.5

–2.0

–2.0 0.0097 0.0102

–2.5

–2.5 0.0096 0.0101

–3.0

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 9.5397×10–3 –3.5 –3.0 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 0.01

3.0

2.0 2.5

0.0414 0.0394

1.5 2.0

0.0393

1.5

1.0 0.0392

0.0412

1.0

0.5 0.0391

0.5

0 0.0410 0.0390

0

0.0408

–1.0 –1.0 0.0388

–1.5 0.0387

–1.5

0.0406 –2.0 0.0386

–2.0

–2.5

0.0385

–2.5 0.0404 –3.0

0.0384

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.0403 –3.5 –3.0 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 0.0384

3.0

2.0 2.5

0.0187

1.5 2.0

0.0172 1.5

1.0

1.0

0.5

0.5

0.0186

0

0

0.0171

–0.5 –0.5

–1.0 –1.0

–1.5

–1.5 0.0185

0.0170 –2.0

–2.0

–2.5

–2.5 –3.0

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.0169 –3.5 –3.0 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 0.0184

Figure 6. Time evolution of whelks’ densities using initial conditions representing Malgas Island, in rectangular (left) and annular (right)

domains. Cases correspond to t = 0, 2, 6 and 10, from top to bottom. Whelk densities are colour coded, from high (red) to low (blue),

within the density scales according to each time point.

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

2.0 10

2.0 0.28

0.28

1.5

1.5

.................................................

0.27

0.27 1.0

1.0

0.26

0

0

0.25 0.25

–0.5

–0.5

–1.0

0.24 –1.0 0.24

–1.5

–1.5

–2.0 0.23 0.23

–2.0

–2.5

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.22 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 0.22

2.0

2.0 0.58 0.85

1.5

1.5

0.80

0.5 0.5

0 0.75

0.75 0

–0.5

–0.5

–1.0 0.70

0.70

–1.0

–1.5

–1.5

–2.0 0.65

0.65

–2.0

–2.5

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.6191 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 0.607

2.0 1.04

2.0

1.02 1.02

1.5

1.5

1.00 1.00

1.0 1.0

0.98

0.5 0.98 0.5

0.96

0 0.96 0

0.94

–0.5

0.94 –0.5

0.92

–1.0

0.92 –1.0 0.90

–1.5

0.88

0.90 –1.5

–2.0

0.86

–2.5 0.88 –2.0

0.84

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 0.8688 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 0.8384

2.0 1.0082

2.0

1.0082

1.5 1.5

1.0080

1.0078

0.5 0.5

1.0078

1.0076

0

0

–0.5 1.0076 1.0074

–0.5

–1.0

1.0072

1.0074 –1.0

–1.5

–1.5 1.0070

–2.0 1.0072

–2.0 1.0068

–2.5

–2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0 1.007 –2.5 –2.0 –1.5 –1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 1.0067

Figure 7. Time evolution of whelks’ densities using initial conditions representing Marcus Island, in rectangular (left) and annular (right)

domains. Cases correspond to t = 0, 0.25, 0.5 and 1, from top to bottom. Whelk densities are colour coded, from high (red) to low (blue),

within the density scales according to each time point.

Downloaded from http://rsos.royalsocietypublishing.org/ on December 26, 2017

Moreover, by introducing spatial variables and letting both populations diffuse within a spatial

11

domain, we obtain patterns that are characteristic of excitable media [19]. Of particular interest are the

columns of ﬁgure 6, where self-sustained waves travel in both the rectangular and annular regions. The

.................................................

latter is not entirely surprising, as the ordinary differential equation model in which the spatial case

was based shows bistability. Nevertheless, our ﬁndings are quite relevant in that, to the best of our

knowledge, there are not many reports of ecological interactions behaving as excitable media so far. The

only other work we are currently aware of is [20], where the authors model ocean plankton populations

as excitable media.

Also, to the best of our knowledge, this is the ﬁrst model proposed to both generate and represent

role-reversals in ecological interactions, and may have wide applicability in explaining—and reverting—

catastrophic shifts in ecosystems [21]. Importantly, role reversal was not introduced explicitly in our

model and was only obtained as a consequence. In other words, our system was constructed using

ecological ﬁrst principles on the rate of change of the variables following ﬁeld observations by Barkai

and McQuaid, and role-reversal was only obtained as a result.

Lastly, it has been argued the creation of predictive models of role-reversal interactions will greatly

alleviate efforts towards preventing ecological collapses or understanding alternative ecosystem states

under changing conditions. The latter is owing to hypothesized path dependencies and ecosystem

hysteresis [22]. Particularly, in marine ecosystems, internal feedback mechanisms have been proposed

to be responsible for fundamental changes in ecosystem properties upon overﬁshing of predators [23].

Thus, a deeper, quantitative understanding of the roles played by species, and their possible exchanges,

becomes essential. The latter will provide better foundation for selective harvesting, hunting and ﬁshing

strategies, leading to more sustainable and predictable ecosystems.

Data accessibility. All additional data supporting this article, including mathematical proofs, have been uploaded as part

of the supplementary material.

Funding statement. P.M. was supported by UNAM-IN107414 funding and wishes to thank OIST hospitality during the

last stages of this work. T.M.L. was supported by OIST funding.

References

1. Wright DH. 1989 A simple, stable model of 9. Saito Y. 1986 Prey kills predator: counter-attack 16. Himmelman JH. 1988 Movement of whelks

mutualism incorporating handling time. Am. Nat. success of a spider mite against its specific Buccinum undatum towards a baited trap. Mar. Biol.

134, 664–667. (doi:10.1086/285003) phytoseiid predator. Exp. Appl. Acarol. 2, 47–62. 97, 521–531. (doi:10.1007/BF00391048)

2. Choh Y, Ignacio M, Sabelis MW, Janssen A. 2012 (doi:10.1007/BF01193354) 17. Lapointe V, Sainte-Marie B. 1992 Currents,

Predator–prey role reversals, juvenile experience 10. Janssen A, Faraji F, van der Hammen T, Magalhaes S, predators, and the aggregation of the gastropod

and adult antipredator behavious. Sci. Rep. 2, 728. Sabelis MW. 2002 Interspecific infanticide deters Buccinum undatum around bait. Mar. Ecol. Prog. Ser.

(doi:10.1038/srep00728) predators. Ecol. Lett. 5, 490–494. (doi:10.1046/j. 85, 245–257. (doi:10.3354/meps085245)

3. Magalhaes S, Janssen A, Monserrat M, Sabelis MW. 1461-0248.2002.00349.x) 18. Powers SS, Kittinger JN. 2002 Hydrodynamic

2005 Prey attack and predators defend: 11. Seitz RD, Lipcius RN, Hines AH, Eggleston DB. 2001 mediation of predator-prey interactions: differential

counterattacking prey trigger parental care in Density-dependent predation, habitat variation, patterns of prey susceptibility and predator success

predators. Proc. R. Soc. B 272, 1929–1933. and the persistence of marine bivalve prey. Ecology explained by variation in water flow. J. Exp. Mar.

(doi:10.1098/rspb.2005.3127) 82, 2435–2451. (doi:10.1890/0012-9658(2001)082 Biol. Ecol. 85, 245–257.

4. Polis GA, Myers CA, Holt RD. 1989 The ecology and [2435:DDPHVA]2.0.CO;2) 19. Krinsky V, Swinney H (eds). 1991 Wave and patterns

evolution of intraguild predation: potential 12. Holbrook S, Schmitt RJ. 2002 Competition for in biological and chemical excitable media.

competitors that eat each other. Annu. Rev. Ecol. shelter space causes density-dependent predation Amsterdam, The Netherlands: North-Holland.

Syst. 20, 297–330. (doi:10.1146/annurev.es.20. mortality in damselfishes. Ecology 83, 2855–2868. 20. Truscott JE, Brindley J. 1994 Ocean plankton

110189.001501) (doi:10.1890/0012-9658(2002)083[2855:CFSSCD] populations as excitable media. Bull. Math. Biol. 56,

5. Dorn NJ, Mittelbach GG. 1999 More than predator 2.0.CO;2) 981–998. (doi:10.1007/BF02458277)

and prey: a review of interactions between fish and 13. Breton LM, Addicott F. 1992 Density-dependent 21. Scheffer M, Carpenter S, Foley JA, Folke C, Walker B.

crayfish. Vie Milieu 49, 229–237. mutualism in an aphid-ant interaction. Ecology 73, 2001 Catastrophic shifts in ecosystems. Nature 413,

6. Palomares F, Caro TM. 1999 Interspecific killing

2175–2180. (doi:10.2307/1941465) 591–596. (doi:10.1038/35098000)

among mammalian carnivores. Am. Nat. 153,

14. Hernandez M, Barradas I. 2003 Variation in the 22. Fauchald P. 2010 Predator–prey reversal: a possible

492–508. (doi:10.1086/303189)

outcome of population interactions: bifurcations mechanism for ecosystem hysteresis in the North

7. Wizen G, Gasith A. 2011 An unprecedented role

and catastrophes. J. Math. Biol. 46, 571–594. Sea? Ecology 91, 2191–2197. (doi:10.1890/09-

reversal: ground beetle larvae lure amphibians and

(doi:10.1007/s00285-002-0192-4) 1500.1)

prey upon them. PLoS ONE 6, e25161. (doi:10.1371/

15. Cobb JS, Phillips BF. 1980 The biology and 23. De Roos AM, Persson L. 2002 Size-dependent

journal.pone.0025161)

8. Barkai A, McQuaid C. 1988 Predator–prey role management of lobsters. Volume I: physiology and life-history traits promote catastrophic collapses of

reversal in a marine benthic ecosystem. Science 242, behaviour. New York, NY: Academic top predators. Proc. Natl Acad. Sci. USA 99,

62–64. (doi:10.1126/science.242.4875.62) Press. 12 907–12 912. (doi:10.1073/pnas.192174199)

- ACSA.AM.86.3Uploaded bybsantacecilia
- Extreme climatic events.pdfUploaded byAnonymous 37PgLC
- askdjfhasl.pdfUploaded byPavan MK
- Lipschitz ConditionUploaded byNuwan Scofield
- Jane LubchencoUploaded byMade Deddy
- Script PDEUploaded byc
- ch1Uploaded byesf_net
- Persistence TutorialUploaded byAngela Yamsuan
- Autonomous EquationsUploaded byAnkitSisodia
- Inter Specific CompetitionUploaded byBlanche Cleo Mayor
- A.new.Class.molecules2006.EUploaded bySergei Ostroumov
- MMChapter6_6p3Uploaded byMuhammad Zulhairi Zulkifli
- 2009 April Malang East Java the Jakarta Globe Students Get Practical Lessons in Ecological Responsibility_1Uploaded byEnvironmental Services Program
- predator-prey populations reportUploaded byapi-456234893
- A 03401001005Uploaded bytheijes
- Math 10Uploaded byAnonymous oM6s8mgs
- 1. DEFINISI EKOLOGIUploaded byekasofarizal
- programmetables12_0Uploaded bybqdianz
- ecosystemsUploaded byVirneDalisay
- Hudson River Sustainable Shorlines Project OverviewUploaded byHRNERR
- 10 29Uploaded byapi-305013025
- Lesson 5 - Part 1: LCMUploaded bymisterreid
- SnS and APGP QuizUploaded byYu Xuan
- evolutionUploaded bypranalinshah
- Reconsidering McHarg[1]Uploaded byMkhahlelwa
- ecology syllabusUploaded byapi-96988934
- Toward a Multicultural EcologyUploaded byaivakhiv
- Report on NZP.docxUploaded byHimanshi Mangla
- 10B. Guattari Remaking Social Practices Copy 2Uploaded byАлександар Гајић
- Exam Final - Notes IIIUploaded byScrewTheSchoolSystem

- 2017 1 INTRODUCCION V5 DIPLOMADO.pdfUploaded byAurivas
- Ejercicios 51 a 100.pdfUploaded byAurivas
- Ejercicios 51 a 100.pdfUploaded byAurivas
- Tablas Frecuencias RUploaded byPablito Roberto
- Calculo3Uploaded byAurivas
- Arcsine Laws and SimuUploaded byAurivas
- Cadenas de MarkovUploaded byFrancisco J. Mejía Cervantes
- clase2019_02_20 AUploaded byAurivas
- Contabilidad Financiera1 Unidad 3Uploaded byZoila
- ProcesosUploaded byAurivas
- Ceva_y_Menelao.pdfUploaded byAurivas
- Teorema Menelao 0001Uploaded byAurivas
- Elon Lages Lima Analisis español!!!!vol1Uploaded byNico Mauricio Soto Mendoza
- Ejercicios 101 Al 180Uploaded byAurivas
- ProbabilityII HW9 SolutionsUploaded byAurivas
- Instructivo Gourmet PlusUploaded byDavid del Prado
- Cuerda s Iguales Arcos 0001Uploaded byAurivas
- Solution's Manual Abstract Algebra RotmanUploaded byplooshhead
- EstDesUploaded byAurivas
- Tablas Frecuencias RUploaded byPablito Roberto
- Encuesta Nacional de Ingresos y Gastos de Los Hogares 2010Uploaded byAurivas
- grafi3[1]Uploaded bywilmer_gonzales_7
- RivasZavala LorenaPatricia M184S4 EnuntiempoUploaded byAurivas
- geo2007.pdfUploaded byAurivas
- Elon Lages Lima Analisis español!!!!vol1Uploaded byNico Mauricio Soto Mendoza
- MarkovUploaded bysergio200800
- symbols-letter.pdfUploaded byAurivas
- GMII_Unidad5.pdfUploaded byAurivas
- GMII_Unidad5.pdfUploaded byAurivas

- Buku Panduan Dell Lattitude E6320Uploaded byRofi Hadi Wibowo
- Keywords in Radical Geography -- An IntroductionUploaded byAndrew Kent
- Survey Mutual-Information-Based Registration of Medical ImagesUploaded byBoda Kishan
- BridgeUploaded byHari Kiran
- chapter 7 electricityUploaded byalia aziz
- the role of self-confidence in enhancing the speaking skillUploaded byDanial Boukha
- ICT- Sinfree GonoUploaded bydnlkaba
- Successful Project ManagementUploaded bye0055996
- MLEUploaded byPoornima Pamulapati
- Diversity StatisticsUploaded byMirela Moldoveanu
- ISJ187Uploaded bynp27031990
- Matthew BrombergerUploaded bydommarajuuu1
- district meeting calendar websiteUploaded byapi-253281432
- Accounting Key FlexfieldUploaded byGopi Krishna Reddy Julakanti
- 9781107596078u10_p92-101Uploaded byStephanie Oliveira Principal
- Consolidated AR 2018Uploaded byJay-ar Jamorabon Torres
- Ed. Change ManagementUploaded bydeutza_hot
- Blue Gene abstractUploaded byBhanu Sai Kolakaleti
- electricity colors.pdfUploaded byeldi_ye
- ideapad_330_15Intel_Platform_SpecificationsUploaded bylegatus2yahoo.gr
- Lm358data SheetUploaded byanon_680632380
- CEL ConsultingUploaded byHuy Tran
- 000 Syllabus (1)Uploaded byGillian Alvero
- ABB rccb f 804Uploaded bycatalincc
- CRM on BanglalinkUploaded byshrjbln
- Maintainance Agreement for WebsitesUploaded byUtkarsh Dubey
- Mechanics of MaterialsUploaded bydanbiasi
- 8254 MicroprocessorUploaded byFaiz Rahman
- Rhetorical Analysis of HappyUploaded byJohn Mccarthy
- SpeakingUploaded byjsayer622