Abstract: In this paper, we extend a Leslie–Gower-type predator–prey system with ratio-dependent Holling III functional response considering the cost of antipredator defence due to fear. We study the impact of the fear effect on the model, and we find that many interesting dynamical properties of the model can occur when the fear effect is present. Firstly, the relationship between the fear coefficient K and the positive equilibrium point is introduced. Meanwhile, the existence of the Turing instability, the Hopf bifurcation, and the Turing–Hopf bifurcation are analyzed by some key bifurcation parameters. Next, a normal form for the Turing–Hopf bifurcation is calculated. Finally, numerical simulations are carried out to corroborate our theoretical results.
Keywords: predator–prey system, the fear effect, Turing instability, Turing–Hopf bifurcation, normal form.
Dynamic analysis of a Leslie–Gower-type predator–prey system with the fear effect and ratio-dependent Holling III functional response

Recepción: 03 Noviembre 2021
Revisado: 23 Abril 2022
Publicación: 29 Junio 2022
As one of the most common mutual relationships between two populations in nature, predator–prey relationship plays a significant role in ecology and mathematical biology [2]. Since the dynamic behaviours of predator–prey models were formulated by Lotka and Volterra, many experts and scholars have studied various types of predator–prey models over the past decades, thus establishing the theoretical basis for interspecific interactions [1, 4, 12, 14]. In 1948, Leslie and Gower introduced a functional response called Leslie– Gower, which was based on the Logistic model proposed by Verhulst. This functional response can be adapted to describe the correlation between a reduction in the number of predators and the per capita availability of the predator’s preferred food [2, 17]. The Leslie–Gower predator–prey system typically takes the following form:
(1)where
is the prey-to-predator conversion factor, and the term
is known as the Leslie–Gower term, which means the scarcity of prey leads to a loss of predator density.
The functional response is an important component of the predator–prey model describing the way in which predator–prey interactions occur. In proposing this function, an essential role is played by the behavior of prey and predator [17,18]. Some common types of functional responses are listed here. For example, Holling I–III functional response [20], Beddington–DeAngelis functional response [10], Leslie–Gower functional response [11], Crowley–Martin functional response [9], and ratio-dependent functional response [6].
The ratio-dependent functional response, a predator-dependent functional response, is an important form in characterizing the functional responses of predator and has a better modeling for a predator–prey system [25]. Based on the existed studies and the above considerations, many experts and scholars have replaced
in (1) with a ratio-dependent functional response and considered its spatial distribution patterns and dispersal mechanisms. Making a suitable nondimensional scaling, system (1) reduces to
(2)where
and
denote, respectively, the densities of the prey and the predator species at the space location
and time
is the Laplacian operator. The positive constants
and
represent separately the diffusion coefficients of the prey and the predator. Parameters
and
are all positive constants. The nonlinear term
in (2) is called ratio-dependent Holling type III functional response [5, 21], and it indicates the growth rate of predator per capita, which is a function of the ratio of the number of prey to predator. The term
is known as the Leslie–Gower term [8], and it means the scarcity of prey leads to a loss of predator density [16]. There have been several reports on the dynamic behavior of this ratio-dependent predator–prey system (2). The Turing and Turing–Hopf bifurcations of system (2) were investigated and the spatiotemporal patterns of system (2) in two-dimensional space were discovered by Chen and Wu [3]. In [16], under homogeneous Neumann boundary conditions, the existence conditions of Hopf bifurcation, Turing instability of spatial uniformity and Turing–Hopf bifurcation in one- dimensional space were shown. In Chang and Zhang [2], they used the Leray–Schauder degree theory and the implicit function theorem to report the nature of the spatially homogeneous Hopf bifurcation and the nonexistence and existence of nonconstant steady states.
In proposing model (2), the fear effect of prey for predator has been neglected. All prey respond to the risk of predation and then exhibit a variety of antipredator responses. The common ones are habitat change, foraging, vigilance, and other different physiological changes [15,19,22–24]. Some previous experimental studies have confirmed this result. In addition, the fear of predation has immense impact on prey species. The mortality of prey is directly increased by predation. Moreover, the fear of prey may affect the physiological condition of juvenile prey, which is harmful to its survival in adulthood, for example, reducing the reproduction of prey [19, 22]. Furthermore, strong behavioral responses can be elicited by the fear of predation enough to affect the population and life history of entire prey populations [13]. According to their ideas [22–24], we extend model (2) by multiplying the production term by a factor
taking in account the cost of antipredator defence due to fear [22], then model (2) becomes
(3)where parameter
refers to the level of fear.
The organizational structure of this paper is as follows. In Section 2, both the existence of positive equilibrium state and the linear stability of system (3) are analysed. Further-more, the bifurcation analysis is investigated in Section 3, where the existence of the Turing bifurcation, the Hopf bifurcation, and the Turing–Hopf bifurcation are shown by choosing the
and
as bifurcation parameters, respectively. Moreover, the normal form of the Turing–Hopf bifurcation with
and
as parameters for system (3) near the unique positive constant equilibrium is obtained in Section 4. Finally, in Section 5, numerical simulations are carried out to verify the obtained theoretical conclusions.
Firstly, the existence of coexisting equilibrium is analyzed by considering the following equation:
(4)Obviously, (1, 0) is a boundary equilibrium point of system (3). In this article, we mainly study the relevant properties of the coexistence equilibrium of system (3). By using the second equation of (4), we are able to obtain
. Substituting this into the first equation of (4), we obtain the expression
.
Theorem 1. The following statements are correct:
Assume that
holds, then
must have a positive real solution.
The equilibrium of prey
is a strictly decreasing function with respect to
when
.
Proof. (i) Obviously,
is a quadratic function of one variable
with the downward opening, and its symmetry axis is
. We can also find
. So there must be a positive solution
to meet
when
(ii) In the case with the fear factor, i.e.,
, for system (3), when
, we can obtain the equilibrium of prey

Simple computation shows

that which indicates that
is a strictly decreasing function with respect to
. That is, increasing the level of
can decrease the value of the prey equilibrium
.
Theorem 1 means that system (3) has a positive equilibrium point. We suppose that
is the positive equilibrium point of system (3) for the remainder of the article. Furthermore, it also means that if the model has a unique positive equilibrium, the fear coefficient
has an effect on the positive equilibrium point: as the fear coefficient
increases, the positive equilibrium point of prey
gradually decreases (see Fig. 1). Next, we conduct a linear stability analysis of system (3). For the positive equilibrium
, the linearized system of (3) is
(5)where

and

It is obvious to know that the characteristic equation of the linearized system (5) is
(6)where


(7)and the eigenvalues of system (3) are given by
(8)Then we make the following hypotheses:

If Assumptions (A1) and (A2) are both valid, then when
, there is
and
, that is to say, the real parts of the eigenvalues of system (3) are all less than zero. Therefore, the following theorem is obtained.
Theorem 2. Suppose that (A1) and (A2) hold. Then the ordinary differential equation system corresponding to system (3) is locally asymptotically stable at the positive equilibrium point
.
In this section, the existence conditions of the Turing instability are analyzed. Under the assumptions that (A1) and (A2) are established, it is known from Theorem 2 that there is
. Then
(see (7)) is selected as the Turing bifurcation line parameter. Let
and discuss in the following three situations:
Case 1. 
Case 2.
and
, where 
Case 3.
and
, where 
After the analysis and discussion of the above three situations, we can get the following theorem.
Theorem 3. Suppose (A1) and (A2) hold. Then the following statements are correct:
In Case 1 or Case 2, the positive equilibrium point
is locally asymptotically stable.
In Case 3, if there does not exist a
such that
then the positive equilibrium point
of system (3) is locally asymptotically stable; conversely, if there exists at least a
such that
then the positive equilibrium point
of system (3) is Turing unstable
Proof. Suppose that (A1) and (A2) hold. Under the condition that the parameters of Case 1 or Case 2 are satisfied, there is
, then if 
, system (3) has the eigenvalue of the negative real part. Then statement (i) is proved. When the parameter relationship belongs to Case 3 and there is not
such that
then a similar method can be used to prove the conclusion. When the parameter relationship belongs to Case 3 and there is
such that
,then the real part of the eigenvalue
of system (3) will be positive, which means that the positive equilibrium point
of system (3) becomes no longer stable. Then the statement (ii) is proved.
Next, we further analyze the necessary conditions and the boundary for the occurrence of Turing instability. Assume that
(B1)
where 
(B2)
where 
We can find that the curve
increases monotonically with
until the first inflection point
, after which the curve
decreases linearly until the second inflection point
, and the value of
is less than zero when
is greater than the second inflectiopoint
. (see Fig. 2(a)). To simplify the study, we only study the part of the curve
before the first inflection point
. In this part,
is monotonically increasing in
and intersects
at the point
. We take 

Hence, we have the following lemma.
Lemma 1. Suppose that (A1) and (A2) hold, then assumptions (B1) and (B2) hold if and only if
.
Proof. Let
, then we can rewrite 
Obviously, the symmetry axis is
, and at this time,
can be taken to the minimum
.
Since
, then
. If we want
with the condition 
must satisfy
Then we can obtain 
When
takes a value on the axis of symmetry,
can be taken to the minimum, and we can get
To ensure that 
is required. Then we can gain
.In the part of the curve
before the first inflection point
increases monotonically with
and intersects with
at the point
, where 

Denote

where
, then
when
. We can find that the curve
increases monotonically with
until the first inflection point
, after which the curve
decreases linearly until the second inflection point
, and the value of
is less than zero when
is greater than the second inflection point
(see Fig. 2(b)). For simplicity, only the part of the curve
before the first inflection point
is studied in this section. Since both
and
are positive parameters, this qualification makes sense.
Lemma 2. Suppose that (A1) and (A2) hold, function
, has the following properties:
increases monotonically with
and intersects 
, and
decreases monotonically as
increases, where
.
For
, the equation
only has one root 
, and 
Define
, then 
. Moreover,
if and only if
.
Theorem 4. Suppose that (A1) and (A2) hold.
For any given
, when
, system (3) occurs Turing bifurcation at the positive equilibrium point
.
, is the critical curve of Turing instability
In Fig. 3(a), we characterize a graph of functions
, and
which will help us understand the results of Lemmas 1 and 2. In Fig. 3(b), we present a graph of the Turing bifurcation line
.


In this section, the existence conditions of the Hopf bifurcation with
as the parameter are first analyzed. Denote

Obviously,
under hypothesis (A2). Denote

After analysis, we can get the following theorem.
Theorem 5. Suppose (A2) holds. System (3) undergoes a Hopf bifurcation at
when
for
. Moreover, the bifurcating periodic solution is spatially homogeneous when
and spatially nonhomogeneous when
for
and 
Proof. Let
be the roots of Eq. (6).
When
we can get
for
, then Eq. (6) has a pair of pure imaginary roots 
When
is near
, from Eq. (8) we can get

Then we can obtain
That is to say, for each
, the transversal condition holds. This completes the proof.
Next, the existence conditions of the Turing–Hopf bifurcation with
and
as parameters are analyzed. System (3) will undergo a Turing–Hopf bifurcation when the following conditions are satisfied:
When
, Eq. (6) has a pair of pure imaginary roots
This phenomenon can be produced when 
When
, Eq. (6) has a single zero root. This phenomenon can be produced when
.
In this section, we assume (A2) always holds. Denote

such that

From the Theorem 5 we can know that system (3) will have a Hopf bifurcation at the positive equilibrium point
when
. Therefore,
when 
are the Turing bifurcation lines, and
is the Hopf bifurcation line. When
, we hope to find the first intersection of these two types of bifurcation lines in the first quadrant as the Turing–Hopf bifurcation point. After the above analysis, we can get the following theorem.
Theorem 6. Suppose hypothesis (A2) holds. For system (3), the following statements are correct:
If
, system (3) does not undergo Turing–Hopf bifurcation.
If
, system (3) undergoes Turing–Hopf bifurcation at the point 
, and the positive equilibrium
of system (3) is locally asymptotically stable when
, where

Proof. In
-plane, the Turing bifurcation curves are

The Hopf bifurcation curve is
.
If
then there is no intersection point between Turing bifurcation curves
and the Hopf bifurcation curve
in the first quadrant. This indicates that system (3) does not undergo Turing–Hopf bifurcation.
If
then the Turing bifurcation curve
and the Hopf bifurcation curve
intersect at point
. This point is called the Turing–Hopf bifurcation point. In addition, when
, it is easy to prove that
for
. Then the positive equilibrium point
is locally asymptotically stable. Next, let us verify the transversality conditions. Suppose
with
when
, and
with
when
, then the transversality conditions are as follows:

This completes the proof.
In this section, the existence conditions of the Hopf bifurcation with
as the parameter are first analyzed. Denote

where

and

Obviously,
under hypothesis (A2). Denote 
. Then we make the following hypotheses:
(C1) 
(C2) 
After analysis, we can get the following theorem.
Theorem 7. Suppose (A2), (C1) and (C2) hold. System (3) undergoes a Hopf bifurcation at
when
for
. Moreover, the bifurcating periodic solution is spatially homogeneous when
and spatially nonhomogeneous when
for
´ and
.
Next, the existence conditions of the Turing–Hopf bifurcation with
and
as parameters are analyzed. In this section, we assume (A2) always holds. Denote

such that

From Theorem 7 we can know that system (3) will have a Hopf bifurcation at
when
. Therefore,
when
are the Turing bifurcation lines, and
is the Hopf bifurcation line. When
, we hope to find the first intersection of these two types of bifurcation lines in the first quadrant as the Turing–Hopf bifurcation point. After the above analysis, we can get the following theorem.
Theorem 8. Suppose hypothesis (A2), (C1), and (C2) hold. For system (3), the following statements are correct:
If
system (3) does not undergo Turing–Hopf bifurcation.
If
system (3) undergoes Turing–Hopf bifurcation at the point 

The proofs of Theorems 7 and 8 are similar to those of Theorems 5 and 6, respectively, and will not be repeated here
In this section, we calculate the normal forms of the Turing–Hopf bifurcation for the reaction–diffusion system (3) at the coexistence equilibrium
. Firstly, we introduce the parameters
and
by letting
and
, which satisfy that the reaction–diffusion system (3) will undergo Turing–Hopf bifurcation at the positive equilibrium point
when
and
. Then system (3) can be transformed into
(9)For system (9),
is still the positive equilibrium point. Let us make the transformations
and
to move
to the origin. After omitting the horizontal bar, system (9) becomes
(10)Then according to [7], for system (10), we can get

where
. Then we can obtain

with


and 
The characteristic matrix corresponding to system (10) is

According to Theorem
are eigenvalues of
, and
is a simple eigenvalue for
with other eigenvalues having negative real parts. Then, by straightforward calculations, we have

Therefore,
and
. satisfying
, where
is the identity matrix. By [7], we can compute the following parameters:

where

According to [7], the normal form restricted to the third order on the central manifold of the reaction–diffusion system (3) at the Turing–Hopf singularity is
(11)Through the parameter transformation
, the normal form equation (11) can be rewritten into real coordinates form (the third-order term is truncated, and the azimuth angle is removed item
)

In this section, we perform the numerical simulations. Taking
, we have
(12)Through calculation, we get the unique positive equilibrium point 
then hypothesis (A2) holds. In addition,
is the Hopf bifurcation curve in
,
-plane.

are the Turing bifurcation curves. Then the normal form restricted on center manifold for the reaction–diffusion system (12) at Turing–Hopf singularity is

Then we have
(13)Considering
, system (13) has equilibria

By [7], we know:
is the coexistence equilibrium;
are spatially inhomogeneous steady states;
is spatially homogeneous periodic solution;
are spatially inhomogeneous periodic solutions.
Then the following critical bifurcation curves can be obtained:

From Fig. 4 it can be seen that the first intersection of the Turing curves
and the Hopf curve
with 
is chosen as the Turing–Hopf bifurcation point. Therefore, system (12) undergoes Turing–Hopf bifurcation at the point
=(0.4052,0.0411). Then the parameter plane partition diagram and phase diagram can be obtained as shown in Fig. 5.


Proposition 1. For given
, the plane of parameters
,
is divided into six regions by bifurcation curves
. For each region, different dynamic phenomenon are generated by system (3). When
, system (3) has a locally asymptotically stable positive equilibrium point
(see Fig. 6). Conversely, when
, the positive equilibrium point
becomes unstable. When
, system (3) has a pair of stable spatially inhomogeneous steady states (see Fig. 7). The spatial patterns and bistability are shown by system (3). When
, there are a pair of stable spatially inhomogeneous periodic solutions and a pair of unstable spatially inhomogeneous steady states (see Fig. 8). When
, there are a pair of stable spatially inhomogeneous periodic solutions, a pair of unstable spatially inhomogeneous steady states, and an unstable spatially homogeneous periodic solution (see Figs. 9 and 10). When
, there are a stable spatially homogeneous periodic solution and a pair of unstable spatially inhomogeneous steady states. There are heteroclinic solutions connecting the unstable spatially inhomogeneous steady state to stable spatially homogeneous periodic solution (see Fig. 11). When
, system (3) has a stable spatially homogeneous periodic solution (see Fig. 12).








In this section, we perform the numerical simulations of Hopf bifurcation with
as the parameter. Taking
, we have
. Through calculation, we get the unique positive equilibrium point
, then hypothesis (A2), (C1), and (C2) hold. Figure 13 shows the numerical simulations of system (3) with Hopf bifurcation.
In this paper, we have formulated a Leslie–Gower-type predator–prey system with the fear effect and ratio-dependent Holling III functional response to consider the cost of fear on prey demography. The main focus of this study is to investigate the influence of antipredator behaviour due to fear of predators analytically and numerically. We obtain many interesting results. Mathematically, we analyze the existence and stability of the positive equilibria of the model and give conditions for the existence of the Turing instability, the Hopf bifurcation, and the Turing–Hopf bifurcation by selecting
,
and
as the bifurcating parameters, respectively. In addition, we calculate the normal form of system (3) and divide the plane of parameters
into six regions
. In each region, we demonstrate that the predator–prey model exhibits complex spatiotemporal dynamics including spatially homogeneous periodic solutions, spatially inhomogeneous periodic solutions, and spatially inhomogeneous steady-state solutions. Ecologically, we show that if the model has a unique positive equilibrium, the fear effect can reduce the density of predator and prey: as the level of fear
increases, both the predator and prey density gradually decrease. Moreover, depending on the predator and prey’s different states in each region, we can give solutions accordingly.
The authors wish to express their gratitude to the editors and the reviewers for the helpful comments.












