Applied Mathematics and Computation 224 (2013) 372–386

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Applied Mathematics and Computation

journal homepage: www.elsevier.com/locate/amc

Modelling and analysis of a delayed predator–prey model with

disease in the predator
Rui Xu ⇑, Shihua Zhang
Institute of Applied Mathematics, Shijiazhuang Mechanical Engineering College, Shijiazhuang 050003, Hebei, PR China

a r t i c l e i n f o a b s t r a c t

Keywords: In this paper, we study a predator–prey model with a transmissible disease spreading in
Eco-epidemiological model the predator population and a time delay representing the gestation period of the predator.
Delay By analyzing corresponding characteristic equations, the local stability of each of feasible
Hopf bifurcation equilibria and the existence of Hopf bifurcations at the disease-free equilibrium and the
LaSalle’s invariance principle
coexistence equilibrium are established, respectively. By means of Lyapunov functionals
Global stability
and LaSalle’s invariance principle, sufficient conditions are derived for the global stability
of the predator-extinction equilibrium and the disease-free equilibrium and the global
attractiveness of the coexistence equilibrium of the system, respectively. Numerical simu-
lations are carried out to support the theoretical analysis.
Ó 2013 Elsevier Inc. All rights reserved.

1. Introduction

Since the pioneering work of Anderson and May [1], great attention has been paid to the modelling and analysis of eco-
epidemiological systems recently (see, for example, [1,2,4,9–14,18,19,21,24,25,27–30,32–35]). An increasing number of
works are devoted to the study of the relationships between demographic processes among different populations and dis-
eases. Most of these works dealt with predator–prey models with disease in the prey (see, for example, [4,10,14,21,27–
30,34]). In [4], Chattopadhyay and Arino considered a predator–prey model with disease in the prey. They assumed that
the sound prey population grows according to a logistic law involving the whole prey population. In [27], Xiao and Chen for-
mulated and analyzed a three species (namely, sound prey (susceptible), infected prey (infective), and predator) eco-epide-
miological system. It was assumed that the disease spreads among the prey population only and the disease is not
genetically inherited. The infected populations do not recover or become immune. They considered the case where the pred-
ator mainly eats only the infected prey. This is in accordance with the fact that the infected individuals are less active and can
be caught more easily, or the behavior of the prey is modified such that they live in parts of the habitat which are accessible
to the predator.
Recently, attention has been paid to the modelling and analysis of eco-epidemiological predator–prey system by assum-
ing that the predator population suffer a transmissible disease (see, for example, [6,9,12,22,23,25,30–32]). In [25], after
reviewing the classical Lotka–Volterra type predator–prey model and SIS epidemic model, Venturino formulated two eco-
epidemiological models with disease in the predators and mass action and standard incidence rates, respectively. In the
two models, it was assumed that the disease spreads among predators only and that the infected individuals do not repro-
duce, only sound ones do. Analysis of the long-term behavior of solutions of the two models was carried out to show that
whether and how the presence of the disease in the predator species affects the behavior of the ecological system, but also
whether the introduction of a sound prey can affect the dynamics of the disease in the predator population. Following the

⇑ Corresponding author.
E-mail address: rxu88@163.com (R. Xu).

0096-3003/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amc.2013.08.067
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 373

work of Venturino [25], in [31], Zhang and Sun considered a predator–prey model with disease in the predator and general
functional response. Sufficient conditions were derived for the permanence of the eco-epidemiological system. In [6], Guo
et al. considered the following eco-epidemiological model:

a12 xðtÞSðtÞ
_
xðtÞ ¼ xðtÞðr  a11 xðtÞÞ  ;
1 þ mxðtÞ
_ a21 xðtÞSðtÞ ð1:1Þ
SðtÞ ¼  r 1 SðtÞ  bSðtÞIðtÞ;
1 þ mxðtÞ
_ ¼ bSðtÞIðtÞ  r2 IðtÞ;
IðtÞ
where xðtÞ; SðtÞ and IðtÞ represent the densities of the prey, susceptible (sound) predator and the infected predator population
at time t, respectively. The parameters a11 ; a12 ; a21 ; m; r; r1 ; r2 and b are positive constants. In system (1.1), the following
assumptions were made:

(A1) In the absence of predation, the prey population xðtÞ grows logistically with the intrinsic growth rate r > 0 and car-
rying capacity r=a11 .
(A2) The total predator population N is composed of two population classes: one is the class of susceptible (sound) pred-
ator, denoted by S, and the other is the class of infected predator, denoted by I.
(A3) The disease spreads among the predator species only by contact and the disease can not be transmitted vertically.
The infected predator population do not recover or become immune. The disease incidence is assumed to be the sim-
ple mass action incidence bSI, where b > 0 is called the disease transmission coefficient.
(A4) Only the susceptible predators have ability to capture prey with Holling type-II response function x=ð1 þ mxÞ; m > 0
is the half saturation rate of the predator and the infected predator are unable to catch prey due to a high infection.
The parameter a12 is the capturing rate of the sound predator, a21 =a12 is the conversion rate of nutrients into the
reproduction of the predator by consuming prey, r1 is the natural death rate of the sound predator, r 2 is the natural
and disease-related mortality rate of the infected predator. Here, r1 6 r2 .

It is well known that time delays of one type or another have been incorporated into mathematical models of population
dynamics by many researchers. We refer to the monographs of Gopalsamy [5], Kuang [15] and MacDonald [16] for general
delayed biological systems and to Beretta and Kuang [3] and Wangersky and Cunningham [26] and references cited therein
for studies on delayed predator–prey systems. In general, delay differential equations exhibit much more complicated
dynamics than ordinary differential equations since a time delay could cause a stable equilibrium to become unstable
and cause the population to fluctuate. Time delay due to gestation is a common example, because generally the consumption
of prey by predator throughout its past history governs the present birth rate of the predator. In [26], Wangersky and Cunn-
ingham proposed and studied the following non-Kolmogorov-type predator–prey model:

_
xðtÞ ¼ xðtÞðr1  axðtÞ  a1 yðtÞÞ;
ð1:2Þ
_
yðtÞ ¼ a2 xðt  sÞyðt  sÞ  r 2 yðtÞ:
This model assumes that a duration of s time units elapses when an individual prey is killed and the moment when the cor-
responding addition is made to the predator population.
In this paper, motivated by the works of Guo et al. [6], Venturino [25] and Wangersky and Cunningham [26], we are con-
cerned with the combined effects of a transmissible disease spreading in predator population by contact and a time delay
due to the gestation of the predator on the global dynamics of a predator–prey system with Holling type-II functional re-
sponse. To this end, we consider the following delay differential equations:

a12 xðtÞSðtÞ
_
xðtÞ ¼ xðtÞðr  a11 xðtÞÞ  ;
1 þ mxðtÞ
_ a21 xðt  sÞSðt  sÞ ð1:3Þ
SðtÞ ¼  r 1 SðtÞ  bSðtÞIðtÞ;
1 þ mxðt  sÞ
_ ¼ bSðtÞIðtÞ  r2 IðtÞ;
IðtÞ
where the parameters a11 ; a12 ; a21 ; m; r; r1 ; r2 and b are the same as that defined in system (1.1), s P 0 represents the time
delay due to the gestation of the sound predator.
The initial conditions for system (1.3) take the form

xðhÞ ¼ /1 ðhÞ; SðhÞ ¼ /2 ðhÞ; IðhÞ ¼ /3 ðhÞ;

ð1:4Þ
/1 ð0Þ > 0; /2 ð0Þ > 0; /3 ð0Þ > 0;
where ð/1 ðhÞ; /2 ðhÞ; /3 ðhÞÞ 2 Cð½s; 0; R3þ0 Þ, the space of continuous functions mapping the interval ½s; 0 into R3þ0 , here
R3þ0 ¼ fðx1 ; x2 ; x3 Þ : xi P 0; i ¼ 1; 2; 3g.
374 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

It is well known by the fundamental theory of functional differential equations [8], system (1.3) has a unique solution
ðxðtÞ; SðtÞ; IðtÞÞ satisfying the initial conditions (1.4). It is easy to show that all solutions of system (1.3) with initial conditions
(1.4) are defined on ½0; þ1Þ and remain positive for all t P 0.
To the best of our knowledge, there have been few works in the literature studying the global stability of the coexistence
equilibrium of an eco-epidemiological model. In the present paper, our primary goal is to carry out a complete mathematical
analysis of system (1.3) and establish its global dynamics. The strategy of proofs utilizes global Lyapunov functionals and
LaSalle’s invariance principle that are motivated by the work in McCluskey [17].
The organization of this paper is as follows. In the next section, by analyzing the corresponding characteristic equations,
we study the local stability of each of feasible equilibria of system (1.3) and the existence of Hopf bifurcations of system (1.3)
at the disease-free equilibrium and the coexistence equilibrium, respectively. In Section 3, by means of Lyapunov functionals
and LaSalle’s invariance principle, we establish sufficient conditions for the global stability of the predator-extinction equi-
librium and the disease-free equilibrium and the global attractiveness of the coexistence equilibrium of system (1.3), respec-
tively. Numerical simulations are carried out in Section 4 to support the main theoretical results. A brief discussion is given
in Section 5 to conclude this work.

2. Local stability and Hopf bifurcations

In this section, we study the local stability of each of feasible equilibria of system (1.3) by analyzing the corresponding
characteristic equations, respectively.
System (1.3) always has a trivial equilibrium E0 ð0; 0; 0Þ and a predator-extinction equilibrium E1 ðr=a11 ; 0; 0Þ. If the follow-
ing holds:

(H1) a21 r > r1 ða11 þ mrÞ,

then system (1.3) has a disease-free equilibrium E2 ðx1 ; S1 ; 0Þ, where

r1 a21 ½a21 r  r 1 ða11 þ mrÞ
x1 ¼ ; S1 ¼ : ð2:1Þ
a21  mr 1 a12 ða21  mr 1 Þ2
Further, it is easy to show that if bS1 > r2 , system (1.3) has a coexistence equilibrium E ðx ; S ; I Þ, where
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
mr  a11 þ ðmr  a11 Þ2 þ 4ma11 ðr  a12 S Þ
x ¼ ;
2ma11 ð2:2Þ
 

r2 1 a21 x
S ¼ ; I ¼  r1 :
b b 1 þ mx
It is easy to prove that the equilibrium E0 ð0; 0; 0Þ is always unstable.
The characteristic equation of system (1.3) at the equilibrium E1 ðr=a11 ; 0; 0Þ is of the form
 
a21 r
ðk þ rÞðk þ r2 Þ k þ r 1  eks ¼ 0: ð2:3Þ
a11 þ mr
Eq. (2.3) always has two negative real roots: k1 ¼ r; k2 ¼ r 2 . All other roots of Eq. (2.3) are determined by the following
equation
a21 r
k þ r1  eks ¼ 0: ð2:4Þ
a11 þ mr
Denote
a21 r
f ðkÞ ¼ k þ r 1  eks :
a11 þ mr
If (H1) holds, it is easy to show that, for k real,
a21 r
f ð0Þ ¼ r 1  < 0; lim f ðkÞ ¼ þ1:
a11 þ mr k!þ1

Hence, f ðkÞ ¼ 0 has a positive real root. Therefore, if (H1) holds, the equilibrium E1 ðr=a11 ; 0; 0Þ is unstable.
If a21 r < r 1 ða11 þ mrÞ, we claim that E1 ðr=a11 ; 0; 0Þ is locally asymptotically stable. Otherwise, there is a root k satisfying
Rek P 0. It follows from (2.4) that
a21 r a21 r
Rek ¼ esRek cosðsImkÞ  r 1 6  r 1 < 0;
a11 þ mr a11 þ mr
which is a contradiction. Hence, if a21 r < r 1 ða11 þ mrÞ, the equilibrium E1 ðr=a11 ; 0; 0Þ is locally asymptotically stable.
The characteristic equation of system (1.3) at the equilibrium E2 ðx1 ; S1 ; 0Þ takes the form
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 375

ðk þ r2  bS1 Þ½k2 þ p1 k þ p0 þ ðq1 k þ q0 Þeks  ¼ 0; ð2:5Þ

where
!
a12 S1
p0 ¼ r 1 r þ 2a11 x1 þ ;
ð1 þ mx1 Þ2
a12 S1
p1 ¼ r þ 2a11 x1 þ þ r1 ;
ð1 þ mx1 Þ2
q0 ¼ r1 ðr þ 2a11 x1 Þ;
q1 ¼ r1 :
Clearly, Eq. (2.5) always has a root k1 ¼ bS1  r2 . All other roots of Eq. (2.5) are determined by the following equation

k2 þ p1 k þ p0 þ ðq1 k þ q0 Þeks ¼ 0: ð2:6Þ

When s ¼ 0, Eq. (2.6) reduces to
k2 þ ðp1 þ q1 Þk þ p0 þ q0 ¼ 0: ð2:7Þ
It is easy to show that
a12 r 1 S1
p0 þ q0 ¼ ;
ð1 þ mx1 Þ2
a12 S1
p1 þ q1 ¼ r þ 2a11 x1 þ :
ð1 þ mx1 Þ2
Hence, if bS1 < r2 and the following hold:

(H2) r þ 2a11 x1 þ a12 S1 =ð1 þ mx1 Þ2 > 0,

the equilibrium E2 is locally asymptotically stable when s ¼ 0.

If ixðx > 0) is a solution of (2.6), separating real and imaginary parts, we have

x2  p0 ¼ q0 cos xs þ q1 x sin xs;

ð2:8Þ
p1 x ¼ q0 sin xs  q1 x cos xs:
Squaring and adding the two equations of (2.8), it follows that
 
x4 þ p21  2p0  q21 x2 þ p20  q20 ¼ 0: ð2:9Þ
By calculation, we derive that
!2
a12 S1
p21  2p0  q21 ¼ r þ 2a11 x1 þ ;
ð1 þ mx1 Þ2
" # ð2:10Þ
a12 S1
p0  q0 ¼ 2r1 r þ 2a11 x1 þ :
2ð1 þ mx1 Þ2

Note that if p0 > q0 , then (H2) holds and p21  2p0  q21 > 0. Hence, if p0 > q0 , Eq. (2.9) has no positive real roots. Accord-
ingly, by Theorem 3.4.1 in Kuang [15] we see that if p0 > q0 and bS1 < r 2 , then E2 is locally asymptotically stable for all s P 0.
If p0 < q0 , then Eq. (2.9) has a unique positive root x0 . That is, Eq. (2.6) has a pair of purely imaginary roots of the form ix0 .
Denote
 
1 q0 x20  p0  p1 q1 x20 2np
sn ¼ arccos þ ; n ¼ 0; 1; 2; . . .
x0 q20 þ q21 x20 x0
By Theorem 3.4.1 in Kuang [15] we see that if bS1 < r2 , p0 < q0 and (H2) hold, then E2 remains stable for s < s0 .
We now claim that
dðRekÞ
j > 0:
ds s¼s0
This will show that there exists at least one eigenvalue with positive real part for s > s0 . Moreover, the conditions for the
existence of a Hopf bifurcation [8] are then satisfied yielding a periodic solution. To this end, differentiating Eq. (2.6) with
respect s, it follows that
376 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

 1
dk 2k þ p1 q1 s
¼ þ  :
ds kðk2 þ p1 k þ p0 Þ kðq1 k þ q0 Þ k

Hence, a direct calculation shows that

  (   ) ( )
1
dðRekÞ dk 2x20 þ p21  2p0 q21
sign ¼ sign Re ¼ sign  2 :
ds k¼ix0 ds ðp0  x20 Þ þ p21 x20 q0 þ q1 x0
2 2 2
k¼ix0

We derive from (2.8) that

 2
p0  x20 þ p21 x20 ¼ q20 þ q21 x20 :
Hence, it follows that
   2 
dðRekÞ 2x0 þ p21  2p0  q21
sign ¼ sign > 0:
ds k¼ix0 q20 þ q21 x20

Therefore, the transversal condition holds and a Hopf bifurcation occurs at x ¼ x0 ; s ¼ s0 .

In conclusion, we have the following results.

Theorem 1. For system (1.3), the following results hold true:

(i) If a21 r < r1 ða11 þ mrÞ, then the equilibrium E1 ðr=a11 ; 0; 0Þ is locally asymptotically stable; if a21 r > r 1 ða11 þ mrÞ, then E1 is
unstable.
(ii) Assume that bS1 < r2 . If p0 > q0 , then the equilibrium E2 ðx1 ; S1 ; 0Þ is locally asymptotically stable for all s P 0; if p0 < q0
and (H2) hold, then there exists a positive constant s0 such that E2 is locally asymptotically stable if 0 < s < s0 and is unstable
if s > s0 . Further, system (1.3) undergoes a Hopf bifurcation at E2 when s ¼ s0 .

The characteristic equation of system (1.3) at the coexistence equilibrium E is of the form

k3 þ P2 k2 þ P1 k þ P 0 þ ðQ 2 k2 þ Q 1 kÞeks ¼ 0; ð2:11Þ
where
!
  a12 S
P0 ¼ r 2 bI r þ 2a11 x þ ;
ð1 þ mx Þ2
!
a21 x a12 S
P1 ¼ r 2 bI þ r þ 2a11 x 
þ ;
1 þ mx ð1 þ mx Þ2
a12 S a21 x ð2:12Þ
P2 ¼ r þ 2a11 x þ þ ;
ð1 þ mx Þ2 1 þ mx
a21 x
Q1 ¼  ðr þ 2a11 x Þ;
1 þ mx
a21 x
Q2 ¼  :
1 þ mx
When s ¼ 0, Eq. (2.11) reduces to
k3 þ ðP2 þ Q 2 Þk2 þ ðP1 þ Q 1 Þk þ P0 ¼ 0:
It is easy to show that if

(H3) r þ 2a11 x þ a12 S =ð1 þ mx Þ2 > 0,

then we have that

a12 a21 x S
P1 þ Q 1 ¼ r 2 bI þ > 0;
ð1 þ mx Þ3
!
a12 a21 x S  a12 S
ðP1 þ Q 1 ÞðP2 þ Q 2 Þ  P0 ¼ r þ 2a11 x þ > 0:
ð1 þ mx Þ3 ð1 þ mx Þ2

Hence, by Routh–Hurwitz criterion we know that if (H3) holds, the equilibrium E is locally asymptotically stable when
s ¼ 0.
Substituting k ¼ ixðx > 0) into (2.11) and separating the real and imaginary parts, one obtains that
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 377

 P2 x2 þ P0 ¼ Q 2 x2 cos xs  Q 1 x sin xs;

ð2:13Þ
x3  P1 x ¼ Q 2 x2 sin xs þ Q 1 x cos xs:
Squaring and adding the two equations of (2.13), it follows that

x6 þ px4 þ qx2 þ r ¼ 0; ð2:14Þ

where

p ¼ P22  2P1  Q 22 ; q ¼ P21  2P0 P2  Q 21 ; r ¼ P20 : ð2:15Þ

2
Letting z ¼ x , Eq. (2.14) can be written as

hðzÞ :¼ z3 þ pz2 þ qz þ r ¼ 0: ð2:16Þ

2
Denote D ¼ p  3q. It is easy to show that if D 6 0, the function hðzÞ is strictly monotonically increasing. If D > 0 and
pffiffiffiffi
pffiffiffiffi

z ¼ D  p =3 < 0 or D > 0; z ¼ D  p =3 > 0 but hðz Þ > 0, then hðzÞ has always no positive roots. Hence, under these
conditions, if (H3) holds, Eq. (2.11) has no purely imaginary roots for any s > 0 and accordingly, the equilibrium E is locally
asymptotically stable for all s P 0.
In what follows, we assume that
pffiffiffiffi

(H4) D > 0; z ¼ D  p =3 > 0; hðz Þ 6 0.

In this case, by Lemma 2.2 in [20], we see that Eq. (2.16) has at least one positive root. Without loss of generality, we
assume that (2.16) has three positive roots, namely, z1 ; z2 and z3 , respectively. Accordingly, Eq. (2.14) has three positive roots
pffiffiffiffiffi
xk ¼ zk ðk ¼ 1; 2; 3Þ.
For k ¼ 1; 2; 3, from (2.13) one can get the corresponding sjk > 0 such that (2.11) has a pair of purely imaginary roots ixk
given by
" #
1 ðP2 Q 2  Q 1 Þx2k þ P1 Q 1  P0 Q 2 2p j
sjk ¼ arccos  þ ; j ¼ 0; 1; . . . : ð2:17Þ
xk Q 22 x2k þ Q 21 xk
Let kðsÞ ¼ v ðsÞ þ ixðsÞ be a root of Eq. (2.11) satisfying v ðsjk Þ ¼ 0; xðsjk Þ ¼ xk .
Differentiating the two sides of (2.11) with respect to s, it follows that
 1
dk 3k2 þ 2P2 k þ P1 2Q 2 k þ Q 1 s
¼ þ  : ð2:18Þ
ds 3 2
kðk þ P 2 k þ P1 k þ P0 Þ 2
kðQ 2 k þ Q 1 kÞ k
After some algebra, one obtains that
  (   )
1
dRek dk
sign ¼ sign Re
ds s¼sj ds
k s¼sjk
(      )
P1  3x2k x2k  P1 þ 2P2 P0  P2 x2k Q 21 þ 2Q 22 x2k
¼ sign   3     : ð2:19Þ
xk  P1 xk 2 þ P0  P2 x2k 2 2
ðQ 2 x2k Þ þ Q 21 x2k
We derive from (2.13) that
 2  2  2
x3k  P1 xk þ P 0  P2 x2k ¼ Q 2 x2k þ Q 21 x2k :
Hence, it follows that
2
3 " #
  3 x4
þ 2 P 2
 2P  Q 2
x2k þ P21  2P0 P2  Q 21 0
dðRekÞ k 2 1 2 h ðzk Þ
sign ¼ sign4 5 ¼ sign :
ds s¼sj Q 22 x4k þ Q 21 x2k Q 22 x4k þ Q 21 x2k
k

From what has been discussed above, we have the following results.

Theorem 2. Let p; q and r be defined in (2.15). Assume that bS1 > r2 and ðH3Þ hold. Then the following results hold true:
pffiffiffiffi
pffiffiffiffi

(i) If D 6 0 or D > 0 and z ¼ D  p =3 < 0 or D > 0; z ¼ D  p =3 > 0 and hðz Þ > 0, then the equilibrium E of system
(1.3) is locally asymptotically stable for all s P 0.
(ii) If (H4) holds, then hðzÞ has at least one positive root zk , and all roots of (2.11) have negative real parts for s 2 ½0; s0k Þ, and the
equilibrium E of system (1.3) is locally asymptotically stable for s 2 ½0; s0k Þ.
0
(iii) If all conditions as stated in (ii) hold true and h ðzk Þ – 0, then system (1.3) undergoes a Hopf bifurcation at E when
j
s ¼ sk ðj ¼ 0; 1; . . .Þ.
378 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

3. Global stability

In this section, we are concerned with the global stability of the coexistence equilibrium E ðx ; S ; I Þ, the disease-free
equilibrium E2 ðx1 ; S1 ; 0Þ and the predator-extinction equilibrium E1 ðr=a11 ; 0; 0Þ of system (1.3), respectively. The strategy
of proofs is to use Lyapunov functional and LaSalle’s invariance principle.
We first give a result on the upper bound of positive solutions of system (1.3) with initial conditions (1.4).

Lemma 3.1. There are positive constants M 1 and M 2 such that for any positive solution ðxðtÞ; SðtÞ; IðtÞÞ of system (1.3) with initial
conditions (1.4),
lim sup xðtÞ < M1 ; lim sup SðtÞ < M 2 ; lim sup IðtÞ < M 2 : ð3:1Þ
t!þ1 t!þ1 t!þ1

Proof. Let ðxðtÞ; SðtÞ; IðtÞÞ be any positive solution of system (1.3) with initial conditions (1.4). Define

a12
VðtÞ ¼ xðt  sÞ þ ðSðtÞ þ IðtÞÞ:
a21
Calculating the derivative of VðtÞ along positive solutions of system (1.3), it follows that
d a12 a12
VðtÞ ¼ xðt  sÞðr  a11 xðt  sÞÞ  ðr 1 SðtÞ þ r 2 IðtÞÞ ¼ r 1 VðtÞ þ xðt  sÞðr þ r 1  a11 xðt  sÞÞ þ ðr1  r2 ÞIðtÞ
dt a21 a21
ðr þ r1 Þ2
6 r 1 VðtÞ þ ;
4a11
which yields lim supt!þ1 VðtÞ 6 ðr þ r 1 Þ2 =ð4a11 r 1 Þ. If we choose

ðr þ r 1 Þ2 a21 ðr þ r 1 Þ2
M1 ¼ ; M2 ¼ ; ð3:2Þ
4a11 r 1 4a11 a12 r 1
then (3.1) follows. This completes the proof. h

Lemma 3.2. For any positive solution ðxðtÞ; SðtÞ; IðtÞÞ of system (1.3) with initial conditions (1.4), we have that
r  a12 M2
lim inf xðtÞ > x :¼ ; ð3:3Þ
t!þ1 a11
where M 2 is defined in (3.2).

Proof. Let ðxðtÞ; SðtÞ; IðtÞÞ be any positive solution of system (1.3) with initial conditions (1.4). By Lemma 3.1 it follows that
lim supt!þ1 SðtÞ 6 M 2 . Hence, for e > 0 being sufficiently small, there is a T 0 > 0 such that if t > T 0 ; SðtÞ < M 2 þ e. Accordingly,
for e > 0 being sufficiently small, we derive from the first equation of system (1.3) that, for t > T 0 ,
_
xðtÞ P xðtÞðr  a11 xðtÞ  a12 ðM 2 þ eÞÞ;
which yields
r  a12 M 2
lim inf xðtÞ P x :¼ :
t!þ1 a11
The proof is complete. h

We are now in a position to state and prove our result on the global stability of the coexistence equilibrium E ðx ; S ; I Þ of
system (1.3).

Theorem 3. Assume that bS1 > r 2 . Then the coexistence equilibrium E ðx ; S ; I Þ of system (1.3) is globally attractive provided
that

(H5) x > r=ð2a11 Þ.

Here, x > 0 is defined in (3.3).

Proof. Let ðxðtÞ; SðtÞ; IðtÞÞ be any positive solution of system (1.3) with initial conditions (1.4). Define
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 379

x
S I
V 11 ðtÞ ¼ k1 x  x  x ln  þ S  S  S ln  þ I  I  I ln  ; ð3:4Þ
x S I
where k1 is a positive constant to be determined later.
Calculating the derivative of V 11 ðtÞ along positive solutions of system (1.3), we derive that
     
d x a12 xðtÞSðtÞ S a21 xðt  sÞSðt  sÞ
V 11 ðtÞ ¼ k1 1  xðtÞðr  a11 xðtÞÞ  þ 1  r1 SðtÞ  bSðtÞIðtÞ
dt x 1 þ mxðtÞ S 1 þ mxðt  sÞ
 
I
þ 1 ½bSðtÞIðtÞ  r 2 IðtÞ: ð3:5Þ
I
On substituting x ðr  a11 x Þ ¼ a12 x S =ð1 þ mx Þ into (3.5), it follows that
    
d x a12 x S x a12 xðtÞSðtÞ
V 11 ðtÞ ¼ k1 1  xðtÞðr  a11 xðtÞÞ  x ðr  a11 x Þ þ  k 1 1 
dt x 1 þ mx x 1 þ mxðtÞ
a21 xðt  sÞSðt  sÞ a21 S xðt  sÞSðt  sÞ
þ  r 1 SðtÞ  þ r 1 S  bI SðtÞ þ r 2 I : ð3:6Þ
1 þ mxðt  sÞ SðtÞð1 þ mxðt  sÞÞ
We rewrite (3.6) as follows
  
d x a12 x S a12 xðtÞSðtÞ
V 11 ðtÞ ¼ k1 1  xðtÞðr  a11 xðtÞÞ  x ðr  a11 x Þ þ  k1 ð1 þ mx Þ þ k1 a12 x SðtÞ
dt x 1 þ mx 1 þ mxðtÞ
a21 xðt  sÞSðt  sÞ a21 S xðt  sÞSðt  sÞ
þ  r 1 SðtÞ  þ r 1 S  bI SðtÞ þ r 2 I : ð3:7Þ
1 þ mxðt  sÞ SðtÞð1 þ mxðt  sÞÞ
Define
V 1 ðtÞ ¼ V 11 ðtÞ þ V 12 ðtÞ; ð3:8Þ
where
Z  
t
xðuÞSðuÞ x S x S ð1 þ mx ÞxðuÞSðuÞ
V 12 ðtÞ ¼ a21   ln  du: ð3:9Þ
ts 1 þ mxðuÞ 1 þ mx 1 þ mx x S ð1 þ mxðuÞÞ
A direct calculation shows that
 
d xðtÞSðtÞ xðt  sÞSðt  sÞ x S xðt  sÞSðt  sÞð1 þ mxðtÞÞ
V 12 ðtÞ ¼ a21  þ ln : ð3:10Þ
dt 1 þ mxðtÞ 1 þ mxðt  sÞ 1 þ mx xðtÞSðtÞð1 þ mxðt  sÞÞ
Letting k1 a12 ð1 þ mx Þ ¼ a21 , we derive from (3.7)–(3.10) that
  
d x a12 x S a21 S xðt  sÞSðt  sÞ
V 1 ðtÞ ¼ k1 1  xðtÞðr  a11 xðtÞÞ  x ðr  a11 x Þ þ  þ r 1 S þ r 2 I 
dt x 1 þ mx SðtÞð1 þ mxðt  sÞÞ
a21 x S xðt  sÞSðt  sÞð1 þ mxðtÞÞ
þ ln
1 þ mx xðtÞSðtÞð1 þ mxðt  sÞÞ
   
x a21 x S x ð1 þ mxðtÞÞ
¼ k1 1  ½xðtÞðr  a11 xðtÞÞ  x ðr  a11 x Þ þ 1 
x 1 þ mx xðtÞð1 þ mx Þ
 
a21 x S ð1 þ mx Þxðt  sÞSðt  sÞ a21 x S a21 x S ð1 þ mx Þxðt  sÞSðt  sÞ x ð1 þ mxðtÞÞ
 þ þ ln þ ln
1 þ mx x SðtÞð1 þ mxðt  sÞÞ 1 þ mx 1 þ mx x SðtÞð1 þ mxðt  sÞÞ xðtÞð1 þ mx Þ
 2  
  

ðx  x Þ a21 x S x ð1 þ mxðtÞÞ x ð1 þ mxðtÞÞ
¼ k1 ½r  a11 ðxðtÞ þ x Þ   1  ln
x 1 þ mx xðtÞð1 þ mx Þ xðtÞð1 þ mx Þ
 
 
a21 x S ð1 þ mx Þxðt  sÞSðt  sÞ

ð1 þ mx Þxðt  sÞSðt  sÞ

  1  ln : ð3:11Þ
1 þ mx x SðtÞð1 þ mxðt  sÞÞ x SðtÞð1 þ mxðt  sÞÞ
Note that the function gðxÞ ¼ x  1  ln x is always non-negative for any x > 0, and gðxÞ ¼ 0 if and only if x ¼ 1. Hence, if
xðtÞ > r=ð2a11 Þ for t P T, we have

ðx  x Þ2
½r  a11 ðx þ x Þ 6 0;
x
with equality if and only if x ¼ x . This, together with (3.11), implies that if xðtÞ > r=ð2a11 Þ for t P T, V 01 ðtÞ 6 0, with equality

ÞxðtsÞSðtsÞ
if and only if x ¼ x ; ð1þmx
x SðtÞð1þmxðtsÞÞ
¼ 1. We now look for the invariant subset M within the set
 
ð1 þ mx Þxðt  sÞSðt  sÞ
M¼ ðx; S; IÞ : x ¼ x ; ¼ 1 :
x SðtÞð1 þ mxðt  sÞÞ
380 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

Since x ¼ x on M and consequently, 0 ¼ xðtÞ _ ¼ x ðr  a11 x  a12 SðtÞ=ð1 þ mx ÞÞ, which yields SðtÞ ¼ S . It follows from the
second equation of system (1.3) that 0 ¼ SðtÞ _ ¼ a21 x S =ð1 þ mx Þ  r 1 S  bS IðtÞ, which leads to I ¼ I . Hence, the only
 
invariant set in M is M ¼ fðx ; S ; I Þg. Therefore, the global attractiveness of E follows from LaSalle’s invariance principle


for delay differential systems (see, for example, Haddock and Terjéki [7]). This completes the proof. h

Theorem 4. Assume that bS1 < r2 . If (H1) and (H5) hold, then the disease-free equilibrium E2 ðx1 ; S1 ; 0Þ of system (1.3) is globally
asymptotically stable.

Proof. It is easy to see that if (H5) holds, then x1 > r=ð2a11 Þ. It follows from (2.10) that p0 > q0 holds. By Theorem 1, we
see that if bS1 < r 2 and (H5) hold, then the equilibrium E2 ðx1 ; S1 ; 0Þ is locally asymptotically stable. Hence, it suffices to
show that all positive solutions of system (1.3) with initial conditions (1.4) converge to E2 . We achieve this by con-
structing a global Lyapunov functional. Let ðxðtÞ; SðtÞ; IðtÞÞ be any positive solution of system (1.3) with initial conditions
(1.4).
Define
 
x S
V 21 ðtÞ ¼ k2 x  x1  x1 ln þ S  S1  S1 ln þ I; ð3:12Þ
x1 S1
where k2 > 0 is a constant to be determined later.
Calculating the derivative of V 21 ðtÞ along positive solutions of system (1.3), it follows that

     
d x1
a12 SðtÞ S1 a21 xðt  sÞSðt  sÞ
V 21 ðtÞ ¼ k2 1  xðtÞ r  a11 xðtÞ  þ 1  r 1 SðtÞ  bSðtÞIðtÞ
dt x 1 þ mxðtÞ S 1 þ mxðt  sÞ
þ bSðtÞIðtÞ  r2 IðtÞ: ð3:13Þ
On substituting x1 ðr  a11 x1 Þ ¼ a12 x1 S1 =ð1 þ mx1 Þ into (3.5), we derive that

 
d x1
a12 x1 S1 x1
a12 xðtÞSðtÞ
V 21 ðtÞ ¼ k2 1  xðtÞðr  a11 xðtÞÞ  x1 ðr  a11 x1 Þ þ  k2 1 
dt x 1 þ mx1 x 1 þ mxðtÞ
a21 xðt  sÞSðt  sÞ a21 S1 xðt  sÞSðt  sÞ
þ  r 1 SðtÞ  þ r 1 S1 þ ðbS1  r 2 ÞIðtÞ: ð3:14Þ
1 þ mxðt  sÞ SðtÞð1 þ mxðt  sÞÞ
Eq. (3.14) can be rewritten as

 
d x1
a12 x1 S1 a12 xðtÞSðtÞ
V 21 ðtÞ ¼ k2 1  xðtÞðr  a11 xðtÞÞ  x1 ðr  a11 x1 Þ þ  k2 ð1 þ mx1 Þ þ k2 a12 x1 SðtÞ
dt x 1 þ mx1 1 þ mxðtÞ
a21 xðt  sÞSðt  sÞ a21 S1 xðt  sÞSðt  sÞ
þ  r 1 SðtÞ  þ r 1 S1 þ ðbS1  r 2 ÞIðtÞ: ð3:15Þ
1 þ mxðt  sÞ SðtÞð1 þ mxðt  sÞÞ
Letting k2 ð1 þ mx1 Þa12 ¼ a21 , it follows from (3.15) that

 
d x1
x1 ð1 þ mxðtÞÞ a12 x1 S1
V 21 ðtÞ ¼ k2 1  ½xðtÞðr  a11 xðtÞÞ  x1 ðr  a11 x1 Þ þ k2 1 þ mx1 
dt x x 1 þ mx1
a21 x1 S1 ð1 þ mx1 Þxðt  sÞSðt  sÞ a21 x1 S1
 þ þ ðbS1  r2 ÞIðtÞ: ð3:16Þ
1 þ mx1 x1 SðtÞð1 þ mxðt  sÞÞ 1 þ mx1
Define

V 2 ðtÞ ¼ V 21 ðtÞ þ V 22 ðtÞ; ð3:17Þ

where
Z t  
xðuÞSðuÞ x1 S1 x1 S1 ð1 þ mx1 ÞxðuÞSðuÞ
V 22 ðtÞ ¼ a21   ln du: ð3:18Þ
ts 1 þ mxðuÞ 1 þ mx1 1 þ mx1 x1 S1 ð1 þ mxðuÞÞ
By calculation we have that
 
d xðtÞSðtÞ xðt  sÞSðt  sÞ x1 S1 xðt  sÞSðt  sÞð1 þ mxðtÞÞ
V 22 ðtÞ ¼ a21  þ ln : ð3:19Þ
dt 1 þ mxðtÞ 1 þ mxðt  sÞ 1 þ mx1 xðtÞSðtÞð1 þ mxðt  sÞÞ
It therefore follows from (3.16)–(3.19) that
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 381

 
d x1
a21 x1 S1 x1 ð1 þ mxðtÞÞ
V 2 ðtÞ ¼ k2 1  ½xðtÞðr  a11 xðtÞÞ  x1 ðr  a11 x1 Þ þ 1
dt x 1 þ mx1 ð1 þ mx1 ÞxðtÞ
a21 x1 S1 ð1 þ mx1 Þxðt  sÞSðt  sÞ a21 x1 S1
 þ þ ðbS1  r 2 ÞIðtÞ
1 þ mx1 x1 SðtÞð1 þ mxðt  sÞÞ 1 þ mx1
 
a21 x1 S1 ð1 þ mx1 Þxðt  sÞSðt  sÞ x1 ð1 þ mxðtÞÞ
þ ln þ ln
1 þ mx1 x1 SðtÞð1 þ mxðt  sÞÞ xðtÞð1 þ mx1 Þ
 
ðxðtÞ  x1 Þ2 a21 x1 S1 x1 ð1 þ mxðtÞÞ x1 ð1 þ mxðtÞÞ
¼ k2 ½r  a11 ðxðtÞ þ x1 Þ   1  ln
xðtÞ 1 þ mx1 ð1 þ mx1 Þx ð1 þ mx1 Þx
 
a21 x1 S1 ð1 þ mx1 Þxðt  sÞSðt  sÞ ð1 þ mx1 Þxðt  sÞSðt  sÞ
  1  ln þ ðbS1  r2 ÞIðtÞ: ð3:20Þ
1 þ mx1 x1 SðtÞð1 þ mxðt  sÞÞ x1 SðtÞð1 þ mxðt  sÞÞ
It follows from (3.20) that if bS1  r 2 < 0, (H1) and (H5) hold true, then V 02 ðtÞ 6 0, with equality if and only if
1 ÞxðtsÞSðtsÞ
x ¼ x1 ; I ¼ 0; ð1þmx
x1 SðtÞð1þmxðtsÞÞ
¼ 1. We now look for the invariant subset M within the set

 
ð1 þ mx1 Þxðt  sÞSðt  sÞ
M¼ ðS; IÞ : x ¼ x1 ; I ¼ 0; ¼1 :
x1 SðtÞð1 þ mxðt  sÞÞ
Since x ¼ x1 on M and consequently, 0 ¼ xðtÞ _ ¼ x1 ðr  a11 x1  a12 SðtÞ=ð1 þ mx1 ÞÞ, which yields S ¼ S1 . Hence, the only invari-
ant set in M is M ¼ fðx1 ; S1 ; 0Þg. Using LaSalle’s invariance principle for delay differential systems, the global asymptotic sta-
bility of the equilibrium E2 of system (1.3) follows. h

Theorem 5. If a21 r 6 r 1 ða11 þ mrÞ, the predator-extinction equilibrium E1 ðr=a11 ; 0; 0Þ of system (1.3) is globally asymptotically
stable.

1.3 1

1.2
0.9
1.1

1 0.8

0.9
0.7
S(t)
x(t)

0.8
0.6
0.7

0.6 0.5

0.5
0.4
0.4

0 50 100 150 200 250 300 350 400 0 50 100 150 200 250 300 350 400
t−x plane t−S plane

0.5

0.45

0.4 0.5

0.35 0.4

0.3 0.3
I(t)
I(t)

0.25 0.2

0.2
0.1
0.15
0
1
0.1
0.8 1.2
1
0.05 0.6 0.8
0.4 0.6
0 0.4
0 50 100 150 200 250 300 350 400 S(t) 0.2 0.2
x(t)
t−I plane

Fig. 1. The temporal solution and phase portrait found by numerical integration of system (1.3) with r ¼ 1:5; a11 ¼ 0:8; a12 ¼ 1:5; a21 ¼ 1;
m ¼ 0:2; r1 ¼ 0:5; r 2 ¼ 0:5; b ¼ 0:5; s ¼ 1:6; ð/1 ; /2 ; /3 Þ  ð0:5; 0:5; 0:5Þ.
382 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

1.3 1

1.2
0.9
1.1

1 0.8

0.9
0.7

S(t)
x(t)

0.8
0.6
0.7

0.6 0.5

0.5
0.4
0.4

0 100 200 300 400 500 0 100 200 300 400 500
t−x plane t−S plane

0.5

0.45

0.4 0.5

0.35 0.4

0.3 0.3
I(t)
I(t)

0.25 0.2

0.2
0.1
0.15
0
1
0.1
0.8 1.5
0.05 0.6 1
0.4 0.5
0
0 100 200 300 400 500 0.2 0
S(t) x(t)
t−I plane

Fig. 2. The temporal solution and phase portrait found by numerical integration of system (1.3) with r ¼ 1:5; a11 ¼ 0:8; a12 ¼ 1:5; a21 ¼ 1; m ¼ 0:2;
r1 ¼ 0:5; r 2 ¼ 0:5; b ¼ 0:5; s ¼ 2:3; ð/1 ; /2 ; /3 Þ  ð0:5; 0:5; 0:5Þ.

Proof. Since the local stability of E1 is established in Theorem 1, it suffices to show that all positive solutions of system (1.3)
with initial conditions (1.4) converge to E1 . Let ðxðtÞ; SðtÞ; IðtÞÞ be any positive solution of system (1.3) with initial conditions
(1.4).
Denote x0 ¼ r=a11 . Define
  Z t
x xðuÞSðuÞ
V 3 ðtÞ ¼ k3 x  x0  x0 ln þ S þ I þ a21 du; ð3:21Þ
x0 ts 1 þ mxðuÞ
where k3 > 0 is a constant to be determined later.
Calculating the derivative of V 3 ðtÞ along positive solutions of system (1.3), we derive that
  
d x0 a12 xðtÞSðtÞ a21 xðtÞSðtÞ
V 3 ðtÞ ¼ k3 1  xðtÞðr  a11 xðtÞÞ  þ  r1 SðtÞ  r 2 IðtÞ: ð3:22Þ
dt xðtÞ 1 þ mxðtÞ 1 þ mxðtÞ
On substituting r ¼ a11 x0 into (3.22), one obtains that
  
d x0 a12 xðtÞSðtÞ a21 xðtÞSðtÞ
V 3 ðtÞ ¼ k3 1  a11 xðtÞðxðtÞ  x0 Þ  þ  r1 SðtÞ  r 2 IðtÞ
dt xðtÞ 1 þ mxðtÞ 1 þ mxðtÞ
a12 xðtÞSðtÞ a21 xðtÞSðtÞ
¼ k3 a11 ðx  x0 Þ2  k3 ð1 þ mx0 Þ þ k3 a12 x0 SðtÞ þ  r 1 SðtÞ  r2 IðtÞ: ð3:23Þ
1 þ mxðtÞ 1 þ mxðtÞ
Letting k3 ð1 þ mx0 Þa12 ¼ a21 , we derive from (3.23) that
d a21 r  r 1 ða11 þ mrÞ
V 3 ðtÞ ¼ k3 a11 ðxðtÞ  x0 Þ2 þ SðtÞ  r 2 IðtÞ: ð3:24Þ
dt a11 þ mr
Let M be the largest invariant subset of fV 03 ðtÞ ¼ 0g. Clearly, if a21 r < r 1 ða11 þ mrÞ, it follows from (3.24) that V 03 ðtÞ 6 0,
with equality if and only if x ¼ x0 ; S ¼ 0; I ¼ 0. If a21 r ¼ r1 ða11 þ mrÞ, we obtain from (3.24) that V 03 ðtÞ ¼ 0 if and only if
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 383

1 0.6

0.55
0.9
0.5
0.8
0.45
0.7
0.4

S(t)
x(t)

0.6 0.35

0.3
0.5
0.25
0.4
0.2
0.3
0.15

0.2 0.1
0 100 200 300 400 500 600 700 800 0 100 200 300 400 500 600 700 800
t−x plane t−S(t)

0.8

0.75
0.8
0.7
0.7
0.65
I(t)

0.6
I(t)

0.6

0.5
0.55

0.5 0.4
0.8
0.6 1
0.45 0.8
0.4
0.6
0.2
0.4 0.4
0 100 200 300 400 500 600 700 800 0 0.2
S(t) x(t)
t−I plane

Fig. 3. The temporal solution and phase portrait found by numerical integration of system (1.3) with r ¼ 0:55; a11 ¼ 0:125; a12 ¼ 1:8; a21 ¼ 1:35;
m ¼ 0:01; r 1 ¼ 0:17; r2 ¼ 0:25; b ¼ 0:95; s ¼ 0:1, ð/1 ; /2 ; /3 Þ  ð0:5; 0:5; 0:5Þ.

x ¼ x0 ; I ¼ 0. Noting that M is invariant, for each element in M, we have xðtÞ ¼ x0 . It therefore follows from the first
equation of system (1.3) that 0 ¼ xðtÞ _ ¼ a12 x0 SðtÞ=ð1 þ mx0 Þ, which yields SðtÞ ¼ 0. Hence, V 03 ðtÞ ¼ 0 if and only if
ðxðtÞ; SðtÞ; IðtÞÞ ¼ ðx0 ; 0; 0Þ. Therefore, the global asymptotic stability of the equilibrium E1 ðr=a11 ; 0; 0Þ follows. This com-
pletes the proof. h

4. Numerical simulations

In this section, we give some examples to illustrate the main results in Sections 2 and 3.

Example 1. In system (1.3), let r ¼ 1:5; a11 ¼ 0:8; a12 ¼ 1:5; a21 ¼ 1; m ¼ 0:2; r1 ¼ 0:5; r2 ¼ 0:5; b ¼ 0:5. It is easy to show that
(H1)-(H2) hold true and p0  q0  0:1361 < 0. Hence, system (1.3) has a disease-free equilibrium E2 ð5=9; 190=243; 0Þ. By
Theorem 1 we see that there exists a positive constant s0 ¼ 1:8766 such that E2 is locally asymptotically stable if 0 < s < s0
and is unstable if s > s0 . Further, system (1.3) undergoes a Hopf bifurcation at E2 when s ¼ s0 . An investigation of system
(1.3) with the coefficients above can be conducted via a numerical integration using the standard MATLAB algorithm (see,
Figs. 1 and 2).

Example 2. In system (1.3), let r ¼ 0:55; a11 ¼ 0:125; a12 ¼ 1:8; a21 ¼ 1:35; m ¼ 0:01; r1 ¼ 0:17; r2 ¼ 0:25; b ¼ 0:95. By calcu-
lation we have S1  0:2972 and bS1  r 2  0:0323. In this case, system (1.3) has a unique coexistence equilibrium
E ð0:6344; 0:2632; 0:7169Þ. By Theorem 2 we see that there exists a positive constant s0 ¼ 0:1688 such that E is locally
asymptotically stable if 0 < s < s0 and is unstable if s > s0 . Further, system (1.3) undergoes a Hopf bifurcation at E when
s ¼ s0 . Numerical simulation illustrates the result above (see, Figs. 3 and 4).
384 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386

3 2.5

2.5
2

2
1.5

S(t)
x(t)

1.5

1
1

0.5
0.5

0 0
0 100 200 300 400 500 600 0 100 200 300 400 500 600
t−x plane t−S plane

1.5

1.5

1
1
I(t)
I(t)

0.5

0.5
0
3
3
2
2
1
1
0
0 100 200 300 400 500 600 0 0
S(t) x(t)
t−I plane

Fig. 4. The temporal solution and phase portrait found by numerical integration of system (1.3) with r ¼ 0:55; a11 ¼ 0:125; a12 ¼ 1:8; a21 ¼ 1:35;
m ¼ 0:01; r1 ¼ 0:17; r2 ¼ 0:25; b ¼ 0:95; s ¼ 0:3, ð/1 ; /2 ; /3 Þ  ð0:5; 0:5; 0:5Þ.

Example 3. In system (1.3), let r ¼ 3; a11 ¼ 5; a12 ¼ 0:3; a21 ¼ 0:3; m ¼ 1; r 1 ¼ 0:1; r2 ¼ 0:15; b ¼ 0:2. It is easy to show that
system (1.3) always has a trivial equilibrium E0 ð0; 0; 0Þ, a predator-extinction equilibrium E1 ð0:6; 0; 0Þ and a disease-free
equilibrium E2 ð0:5; 2:5; 0Þ. Clearly, bS1  r 2 ¼ 0:35. Hence, system (1.3) has a unique coexistence equilibrium
E ð0:5714; 0:75; 0:0454Þ. The equilibria E0 ; E1 and E2 are always unstable. A direct calculation shows that Eq. (2.14) has three
roots: 7:8679 and 0:0010  0:0009i. Therefore, the equilibrium E is locally asymptotically stable for all s P 0. It is easy to
show that x ¼ 0:3117 > 0:3 ¼ r=ð2a11 Þ. By Theorem 3, we see that the equilibrium E is globally stable. Numerical simulation
illustrates the result above (see, Fig. 5).

5. Discussion

In this paper, we have investigated the global dynamics of a predator–prey model with a disease that can be transmitted
by contact spreading among the predator population and a time delay representing the gestation period of the predator. By
analyzing the corresponding characteristic equations, the local stability of each of feasible equilibria has been established,
respectively. It has been shown that, under some conditions, the time delay due to the gestation of the predator may desta-
bilize both the disease-free equilibrium and the coexistence equilibrium of the eco-epidemiological system and cause the
population to fluctuate. By comparison argument, a priori lower bound of the density of the prey population was derived.
By means of Lyapunov functional and LaSalle’s invariance principle, sufficient conditions were obtained for the global
asymptotic stability of the coexistence equilibrium, the disease-free equilibrium and the predator-extinction equilibrium
of system (1.3), respectively. By Theorem 3 we see that if the prey population is always abundant enough and the disease
transmission coefficient b is sufficiently large, the coexistence equilibrium is a global attractor of the system (1.3). In this
case, the disease spreading in the predator becomes endemic and the prey, sound predator and the infected predator coexist.
By Theorem 4 we see that if the disease transmission coefficient b is sufficiently small and the prey population is always
abundant enough, the disease among the predator population dies out and in this case, the prey and the sound predator
 R. Xu, S. Zhang / Applied Mathematics and Computation 224 (2013) 372–386 385

0.7 2.5

0.6
2

0.5

1.5
0.4

S(t)
x(t)

0.3
1

0.2

0.5
0.1

0 0
0 2000 4000 6000 8000 10000 0 2000 4000 6000 8000 10000
t−x plane t−S plane

0.9

0.8 1

0.7 0.8

0.6 0.6
I(t)
I(t)

0.5 0.4

0.4
0.2
0.3
0
3
0.2
0.8
2
0.1 0.6
1 0.4
0 0.2
0 2000 4000 6000 8000 10000 0 0
S(t) x(t)
t−I plane

Fig. 5. The temporal solution and phase portrait found by numerical integration of system (1.3) with r ¼ 3; a11 ¼ 5; a12 ¼ 0:3; a21 ¼ 0:3; m ¼ 1;
r1 ¼ 0:1; r 2 ¼ 0:15; b ¼ 0:2; s ¼ 2; ð/1 ; /2 ; /3 Þ  ð0:01; 0; 01; 0; 01Þ.

coexist. We rewrite a21 r 6 r 1 ða11 þ mrÞ as a21 6 r 1 ðm þ a11 =rÞ. By Theorem 5 wee see that if the carrying capacity of the prey
and the conversion rate of the predator are sufficiently small, and the death rate of the sound predator and the half satura-
tion rate of the predator are sufficiently large, the prey population persists and the predator population goes to extinction.
There have been a few works on the effects of transmissible disease spreading among predator population and time delay
due to gestation on the dynamics of predator–prey systems (see, for example, [30,32]). In these works, by regarding the delay
as the bifurcation parameter and analyzing the characteristic equation of the linearized system of the original system at the
coexistence equilibrium, the local asymptotic stability of the coexistence equilibrium and the existence of Hopf bifurcation
were investigated. Little attention has been paid to the global stability of the coexistence equilibrium. To the best of our
knowledge, mathematically, Theorem 3 in the present work is the first result on the global stability of a unique coexistence
equilibrium for eco-epidemiological predator–prey models with disease in the predator and time delay due to gestation of
the predator. The proof relies on the construction of a global Lyapunov functional. Establishing global stability is crucial for
our study, since local stability cannot rule out the possibility of periodic solutions far away from equilibria. Mathematically,
the Lyapunov functionals in this paper would be successfully applied in the other biological dynamic models with discrete
delays and even with distributed delays.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 11071254), the Scientific Research
Foundation for the Returned Overseas Chinese Scholars, State Education Ministry and the Natural Science Foundation of
Young Scientist of Hebei Province (No. A2013506012).

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