
This paper presents a mathematical model to describe the spread of flavescence dorée, a disease caused by the bacterium Candidatus Phytoplasma vitis, which is transmitted by the insect vector Scaphoideus titanus in grapevine crops. The key contribution of this work is the derivation of conditions under which positive periodic solutions exist. These conditions are based on the assumption that key factors such as recruitment rates, disease transmission, and vector infectivity vary periodically, thus reflecting seasonal changes. The existence of these periodic solutions is proven using the degree theory, and numerical examples are provided to support the theoretical findings. This model aims to enhance the understanding of the epidemiological dynamics of flavescence dorée and contribute to developing better control strategies to manage the disease in grapevines.
Citation: Fernando Huancas, Aníbal Coronel, Rodolfo Vidal, Stefan Berres, Humberto Brito. A mathematical model of flavescence dorée in grapevines by considering seasonality[J]. Mathematical Biosciences and Engineering, 2024, 21(11): 7554-7581. doi: 10.3934/mbe.2024332
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This paper presents a mathematical model to describe the spread of flavescence dorée, a disease caused by the bacterium Candidatus Phytoplasma vitis, which is transmitted by the insect vector Scaphoideus titanus in grapevine crops. The key contribution of this work is the derivation of conditions under which positive periodic solutions exist. These conditions are based on the assumption that key factors such as recruitment rates, disease transmission, and vector infectivity vary periodically, thus reflecting seasonal changes. The existence of these periodic solutions is proven using the degree theory, and numerical examples are provided to support the theoretical findings. This model aims to enhance the understanding of the epidemiological dynamics of flavescence dorée and contribute to developing better control strategies to manage the disease in grapevines.
In recent decades, agricultural exports have become a critical driver of economic growth for many countries, with the wine industry being one of its crucial components [1,2,3,4,5]. It is well-known that the wine industry, along with businesses and grape agriculture, involves many stakeholders and has attracted diverse perspectives from science and technology. Approaches related to climate change, organic production, and sustainability have increasingly shaped practices in the wine industry [6,7,8]. Furthermore, vineyards contribute to wine production and serve as a source of income for the tourism sector, thus creating employment and fostering economic development in rural areas where vineyards are located. Overall, vineyards hold a significant role in global agriculture, thereby offering economic, cultural, and social benefits across various regions of the world. These facts underscore the importance of research and innovation to ensure the sustainability of the industry [9,10]. In this work, we focus specifically on diseases that affect vineyards, as understanding the dynamics of these diseases is crucial for sustainable production and reducing pesticide use, which, in turn, minimizes the environmental impact and production costs [11,12,13,14,15]. Epidemiology, traditionally seen as a descriptive science focused on the ecological factors of diseases, has evolved significantly in recent years. Now, it incorporates more advanced analytical methods, among which mathematical modeling plays a key role [16]. The modeling of infectious disease transmission in human populations has been extensively studied [17,18,19,20,21], and its importance became even more apparent during the COVID-19 pandemic, which highlighted the need for models to inform immediate public health measures [20]. The methodologies used to model human diseases can be generalized to other populations, including animals and plants [16,19,22].
A commonly used approach is the compartmental model, which divides the total population into sub-populations (often susceptible, infected, and recovered classes) and uses the laws of interaction and mass conservation to describe the system [23,24,25,26,27]. This methodology can be adapted to model the interaction between two populations, such as animals and plants, to study diseases caused by pathogens such as bacteria, viruses, fungi, and other microscopic organisms [28,29,30,31,32,33]. In the context of plant diseases, the spread is often modeled through vector-host interactions, where the vector transmits the disease between hosts, as is the case with many vector-borne diseases [28,29,34].
In this study, we focus on one such vector-borne disease that affects grapevines: flavescence dorée, that affects caused by the bacterium Candidatus Phytoplasma vitis and transmitted by the insect vector Scaphoideus titanus. The role of Scaphoideus titanus in transmitting flavescence dorée was first proposed in [34], and has since been confirmed in various studies [30]. This leafhopper feeds on the sap of grapevines, acquiring the bacteria from infected plants and transmitting it to healthy ones, thus facilitating the spread of the disease. Flavescence dorée severely impacts the grapevine health and yield, that affects presenting symptoms such as leaf yellowing, stunted growth, and wilting of the grape clusters. Over time, it can also damage the wood tissue of grapevines, thus leading to a significant reduction in grape production.
In order to introduce the results of the paper, we first provide the assumptions and the mathematical model. We consider the interaction of two populations: grapevines and vectors, with the total populations denoted by P and V, respectively. The grapevine population is divided into three compartments: Ps, Pe, and Pi, which represent the number of grapevines that are susceptible to infection, exposed to the bacterium via the vector but not yet infective, and infected and infective, respectively. The vector population, denoted by V, is subdivided into three compartments: susceptible, exposed, and infected, denoted by Vs, Ve, and Vi, respectively. We assume that the total grapevine population, P=Ps+Pe+Pi, remains constant throughout the epidemic, as grapevines have a much longer life cycle than the vectors. In contrast, the vector population, V=Vs+Ve+Vi, is variable. The dynamics and interactions of these two populations are modeled based on the following assumptions:
(ⅰ) The birth and mortality rates of the vectors are given by Λ and μ(V)=μ1+μ2V, respectively, where (μ1)−1 is the average lifespan of a vector, and μ2V represents the mortality coefficient, which is proportional to the number of vectors. Thus, V′(t)=ΛV−μ(V)V describes the vector population dynamics.
(ⅱ) The infection force from the grapevine to the vector, denoted by ΦP, is defined as the rate at which the susceptible vectors become infected per unit of time. It is the product of the number of plants N visited by a vector per unit of time, the probability that a plant is infective (Pi/P), and q, which represents the probability of transmission of the bacterium from the plant to the vector. Hence, ΦP=NqPi/P, and the number of newly infected vectors per unit of time is given by ΦPVs=qNVsPi/P.
(ⅲ) The infection force from the vector to the grapevine, denoted by ΦV, is defined as the rate at which susceptible grapevines are infected per unit of time. It is determined by the number of vectors which visit a plant per unit time, NV/P, the probability that a vector is infective (Vi/V), and q∗, which represents the probability of transmission of the bacterium to the grapevine. Therefore, ΦV=q∗(NV/P)(Vi/V), and the number of newly infected grapevines per unit of time is ΦVPs=q∗NViPs/P.
(ⅳ) The parameters involved in the dynamics are α, γ, θ, and κ, which represents the rate at which exposed grapevines become infective, the rate at which infected grapevines recover and become susceptible again, the rate at which exposed vectors become infective, and the rate at which infected vectors recover, respectively. We note that (α)−1 is the average incubation period of the bacterium in the grapevine, (γ)−1 is the average infectious period of the grapevine, (θ)−1 is the average incubation period of the bacterium in the vector, and (κ)−1 is the average recovery time of the vector.
A schematic representation of the model is provided in Figure 1, and a summary of the notation is given in Table 1. Additionally, it is well-established that climate has a significant impact on the population dynamics of insects, which act as carriers for the bacterium Candidatus Phytoplasma vitis, which is the causal agent of flavescence dorée disease [11,35,36,37,38]. Consequently, the inclusion of periodicity in the model allows us to account for seasonal variations that affect the spread of the disease, which ultimately leads to more effective and precise strategies to manage grapevine crops. For this reason, we assume that the parameters β, α, Λ, ν, θ, μ, and κ vary over time, following a non-negative, ω-periodic pattern.
Ps | Number of susceptible grapevines | (α)−1 | Average incubation time on grapevine |
Pe | Number of exposed grapevines | (γ)−1 | Average recovery time of infected grapevines |
Pi | Number of infected grapevines | μ | Mortality rate of vectors |
Vs | Number of susceptible vectors | (θ)−1 | Average incubation time in vector |
Ve | Number of Exposed Vectors | (κ)−1 | Average time of vector infection |
Vi | Number of infected vectors | (ν)−1 | Transmission rate of vectors |
Λ | Average insect vector birth rate | P | Total number of grapevines |
β | Infection rate of grapevines by vectors | V | Total number of vectors |
According to the hypotheses and the previously notation introduced, the dynamics of flavescence dorée propagation in a grapevine population can be modeled by the following system of non-linear differential equations:
dPs(t)dt=−β(t)Vi(t)Ps(t)P+γ(t)Pi(t), | (1.1) |
dPe(t)dt=β(t)Vi(t)Ps(t)P−α(t)Pe(t), | (1.2) |
dPi(t)dt=α(t)Pe−γ(t)Pi, | (1.3) |
dVs(t)dt=Λ(t)V(t)−(μ1(t)+μ2(t)V(t))Vs(t)−ν(t)Vs(t)Pi(t)P+κ(t)Vi(t), | (1.4) |
dVe(t)dt=−(μ1(t)+μ2(t)V(t))Ve(t)+ν(t)Vs(t)Pi(t)P−θ(t)Ve(t), | (1.5) |
dVi(t)dt=−(μ1(t)+μ2(t)V(t))Vi(t)+θ(t)Ve(t)−κ(t)Vi(t). | (1.6) |
The system (1.1)–(1.6) is supplemented by the following initial conditions:
Ps(0)=P0s,Pe(0)=P0e,Pi(0)=P0i,Vs(0)=V0s,Ve(0)=V0e,Ve(0)=V0i. | (1.7) |
The system (1.1)–(1.6) generalizes the model proposed in [28], where the case with constant coefficients was studied. It is important to note that P is constant, and V satisfies a logistic-type equation with variable coefficients: V′(t)=[Λ(t)−(μ1(t)+μ2(t)V(t))]V(t).
In this paper, we propose and prove three main results. First, we introduce sufficient conditions for the existence of positive periodic solutions for the model (1.1)–(1.7) (see Theorem 1.1). Second, we establish the existence of a solution for the operator equation (see Theorem 1.2). Finally, we present numerical results to demonstrate the theoretical findings (see Section 5).
We begin by introducing the notation for the space of periodic functions. Specifically, we consider the Banach space E, defined as the space of continuous and ω-periodic functions, defined as the following set:
E={x∈C0(R;R6):x(t+ω)=x(t),‖x‖:=6∑i=1maxt∈[0,ω]|xi(t)|<∞}. | (1.8) |
The following theorem provides the result for the existence of positive periodic solutions for the system (1.1)–(1.7):
Theorem 1.1. Let E the space defined in (1.8). Assume that the initial conditions are positive (P0s,P0e,P0i,V0s,V0e,V0i)∈R6+, and the coefficients β,α,γ,Λ,μ1,μ2,θ,κ, and ν are non-negative ω−periodic functions, with Λ and μ1 satisfying the relation (Λ−μ1)(t)≥0 for t∈[0,ω]. Then, the system (1.1)–(1.7) admits at least one ω−periodic solution.
The methodology used to prove Theorem 1.1 is based on the topological degree theory, specifically Mawhin's Continuation Theorem [39] (see also [40,41]). Applications of the topological degree theory to epidemiology were recently conducted in [42,43,44]. If we define Dom(L)=E∩C1(R;R6) and introduce the the operators L and N:Dom(L)⊂E→E by the following relations,
L(x)=(dxdt), | (1.9) |
N(x)=(−β(t)ex6+γex3−x1,β(t)ex6+x1−x2−α,αex2−x3−γ,Λ(t)(ex4+ex5+ex6)e−x4−(μ1+μ2P(ex4+ex5+ex6))−ν(t)ex3+κex6−x4,−(μ1+μ2P(ex4+ex5+ex6))+ν(t)ex3+x4−x5−θ,−(μ1+μ2P(ex4+ex5+ex6))+θex5−x6−κ), | (1.10) |
then we observe that the system (1.1)–(1.7) can be written as the following operator equation:
Lx=Nx. | (1.11) |
The rewritten version of (1.1)–(1.7) as the operator equation (1.11) is obtained by introducing x(t)=(x1,…,x6)(t) by the following relation
(Ps,Pe,Pi,Vs,Ve,Vi)(t)=(Pex1(t),Pex2(t),Pex3(t),Pex4(t),Pex5(t),Pex6(t)). | (1.12) |
More precisely, we have that the following three statements are true: (ⅰ) x is a solution of the operator equation (1.11) if and only if a solution of (Ps,Pe,PI,Vs,Ve,Vi)T(t) is a solution of the system (1.1)–(1.7); (ⅱ) if the solution of (1.11) is ω−periodic, then the solution of system (1.1)–(1.7) is also ω−periodic; and (ⅲ) if operator equation (1.11) has a solution, the system (1.1)–(1.7) has a positive solution (see Appendix A). Thus, the analysis of the positive periodic solutions of (1.1)–(1.7) is reduced to obtain the existence of solutions of the operator equation (1.11), which will be performed by applying the topological degree theory.
Theorem 1.2. Consider that the hypotheses of Theorem 1.1 are satisfied, and let L and N be the operators defined in (1.9) and (1.10), respectively. Let Ω⊂E denote the open ball in E centered at 0∈E with radius σ. That is, Ω is the following set:
Ω={x∈E:‖x‖<σ}. | (1.13) |
Then, there exists a solution to the operator equation (1.11).
We note that the radius σ will be defined in terms of the bounds of the coefficients in the mathematical model (1.1)–(1.7).
In the other part of the main results, we consider parameters that arise from experimental data and introduce numerical simulations in which the coefficients are treated as periodic functions.
The article is organized as follows. In Section 2, we recall the definitions and results of Mawhin's degree of coincidence theory, using the framework presented in [39,40]. In Sections 3 and 4, we present the proofs of Theorems 1.2 and 1.1, respectively. In Section 5, we provide numerical examples. In Section 6, we present the conclusions and outline some directions for future work. Moreover, in Appendix A, we provide the details of the reformulation of the system (1.1)–(1.7) as operator equation, and prove some properties of the operators L and N defined in (1.9) and (1.10), respectively.
In this section, we introduce the notation, terminology, and relevant results of the topological degree theory that are necessary for proving Theorem 1.1 through the application of Mawhin's Continuation Theorem [39,40,41]. Moreover, we present some properties of operators the L and N defined in (1.9) and (1.10), respectively.
Let us consider X and Z, which are two Banach spaces with norms ‖⋅‖X and ‖⋅‖Y, respectively; L:Dom(L)⊂X→Z and L:X→Z be two operators; and Ω⊂E be an open bounded set. We assume that L is a linear Fredholm operator of index zero, namely, Im(L) is closed in Z and dim(Ker(L))=codim(Im(L))<∞. It is well-known that there exists the continuous projectors P:X→X and Q:Z→Z such that the following assertions are satisfied
Im(P)=Ker(L),Im(L)=Ker(Q)=Im(I−Q),there exists KP:Im(L)→Dom(L)∩Ker(P) such thatLKpx=x for all x∈Im(L) and PKp=0,there exists an isomorphism J:Im(Q)→Ker(L).} | (2.1) |
Meanwhile, we consider that the operator N:E→F is L−compact on ¯Ω (i.e., N is continuous, QN(¯Ω) is bounded, and KP(I−Q)N is compact on the set ¯Ω).
On the other hand, we recall the definition of the degree of a function. Let U⊂Rn be an open and bounded set, f:U→Rn be a given function, and define the set Nf={x∈U:Jf(x)=0}, where Jf(x) denotes the Jacobian of f at x. If f∈C1(U,Rn)∩C(¯U,Rn) and y∈Rn∖f(∂U∪Nf), then
deg{f,U,y}={∑x∈f−1(y)sgnJf(x),f−1(y)≠∅,0,f−1(y)=∅, | (2.2) |
defines the degree of f on U at y.
The following theorem, often referenced as Mawhin's Continuation Theorem, establishes the specific assemblage of properties of the operators L and N, which are needed to prove the existence of the solution of the operator equation (1.11).
Theorem 2.1. Assume that X and Y are Banach spaces, Ω⊂X is and open bounded set, L:Dom(L)⊂X→Y is a Fredholm mapping of index zero, and N:X→Y is a L−compact operator on ¯Ω. If the following hypotheses are met:
(C1) For each (λ,x)∈(0,1)×(∂Ω∩Dom(L)), the relation Lx≠λNx is satisfied.
(C2) For each x∈∂Ω∩Ker(L), the relation QNx≠0 is satisfied.
(C 3) deg(JQN,Ω∩Ker(L),0)≠0.
then there exists at least one x∈Dom(L)∩¯Ω satisfying the operator equation Lx=Nx.
Let us consider that X=Y=F and L and N are the operators defined in (1.9) and (1.10). We observe that L and N satisfy the hypotheses of Theorem 2.1. More precisely, we have the following Lemma (for details of the proof see Appendix B).
Lemma 2.1. Let us consider the operators L and N give by the relations on (1.9) and (1.10), respectively, with X=Y=F defined in (1.8) and Ω be the set given in (1.13). Then, the following assertions are satisfied
(a) L is a Fredholm operator of index zero with KerL≅R6 and Im(L)={y∈F:∫ω0y(τ)dτ=0}.
(b) N is a continuous operator.
(c) Let P:F→F defined by P(x)=ω−1∫ω0x(τ)dτ. Then, the relations (2.1) are satisfied if we select P=Q.
(d) If the assumptions of Theorem 1.1 are fulfilled, then the operator N is L-compact on ¯Ω.
Hereinafter, we use the notation ‖⋅‖∞ for ‖⋅‖L∞([0,ω]).
Proposition 3.1. Let L and N be the operators defined in (1.9) and (1.10), respectively, and consider the following notation:
V__=V0s+V0e+V0iP[(V0s+V0e+V0i)exp(‖Λ−μ1‖∞ω)‖μ2‖∞ω+1], | (3.1) |
¯¯V=V0s+V0e+V0iPexp(‖Λ−μ1‖∞ω)‖μ2‖∞ω. | (3.2) |
If λ∈(0,1) and the assumptions of Theorem 1.1 are satisfied, then the following relations
ex1(t)+ex2(t)+ex3(t)=1,ex4(t)+ex5(t)+ex6(t)∈[V__,¯¯V],t∈[0,Ω] | (3.3) |
are satisfied for any x solution of the system Lx(t)=λNx(t).
Proof. In order to prove (3.3), we multiply each equation of the system Lx(t)=λNx(t) by exi(t); by regrouping and adding the resulting equations, we deduce the following
ddt(ex1+ex2+ex3)=0, | (3.4) |
ddt(ex4+ex5+ex6)=λ(Λ−μ1)(t)(ex4+ex5+ex6)−λμ2(t)P(ex4+ex5+ex6)2. | (3.5) |
From (3.4) and the integration on [0,t], we deduce the first relation in (3.3), since
ex1(t)+ex2(t)+ex3(t)=ex1(0)+ex2(0)+ex3(0)=P0sP+P0eP+P0iP=P0s+P0e+P0iP=1. |
Similarly, by integration of (3.5) as a Bernoulli equation, we obtain the following
ex4(t)+ex5(t)+ex6(t)=(ex4(0)+ex5(0)+ex6(0))exp(∫t0λ(Λ−μ1)(s)ds)(ex4(0)+ex5(0)+ex6(0))Pλ∫t0exp(∫s0λ(Λ−μ1)(τ)dτ)μ2(s)ds+1=(V0s+V0e+V0i)exp(∫t0λ(Λ−μ1)(s)ds)P[(V0s+V0e+V0i)λ∫t0exp(∫s0λ(Λ−μ1)(τ)dτ)μ2(s)ds+1]⋅ | (3.6) |
From the hypothesis of Theorem 1.1, we have that 0≤mint∈[0,ω]λ(Λ−μ1)(t)≤λ(Λ−μ1)(t)≤‖Λ−μ1‖∞ for t∈[0,ω]. Then, using the increasing behavior of the exponential function and the fact that λ∈(0,1), we obtain the following inequality:
1≤exp(mint∈[0,ω]λ(Λ−μ1)(t))≤exp(∫t0λ(Λ−μ1)(s)ds)≤exp(‖Λ−μ1‖∞ω),t∈[0,ω]. | (3.7) |
Considering s instead of t in the upper limit of the integral given on the estimate (3.7), and multiplying by μ2(s) and integrating on [0,t]⊂[0,ω], we deduce the following:
0≤tmint∈[0,ω]μ2(t)≤tmint∈[0,ω]μ2(t)exp(mint∈[0,ω]λ(Λ−μ1)(t))≤λ∫t0exp(∫s0λ(Λ−μ1)(τ)dτ)μ2(s)ds≤exp(‖Λ−μ1‖∞ω)‖μ2‖∞ω,t∈[0,ω], |
which implies the following estimates
1≤(V0s+V0e+V0i)λ∫t0exp(∫s0λ(Λ−μ1)(τ)dτ)μ2(s)ds+1≤(V0s+V0e+V0i)exp(‖Λ−μ1‖∞ω)‖μ2‖∞ω+1,t∈[0,ω]. | (3.8) |
From (3.7) and (3.8) in (3.6), we deduce the second relation in (3.3).
Proposition 3.2. [42] Let Ψ:[0,ω]⊂R+→R be a function such that is absolutely continuous and satisfies the following differential inequality:
ddtΨ(t)+m(t)Ψ(t)≥0,∀t∈[0,ω], | (3.9) |
for a function m∈L1([0,ω]) which is bounded on [0,ω] (i.e., there exists m1,m2∈R+ such that 0<m1≤m(t)≤m2 for all t∈[0,ω]). Then, the assumption Ψ(0)>0 implies the estimate Ψ(t)≥Ψ(0)exp(−m2ω)>0 for all t∈[0,ω].
Lemma 3.1. Assume that the hypotheses of Lemma 2.1 and Theorem 1.1 are satisfied. Additionally, if (λ,x)∈(0,1)×(∂Ω∩Dom(L)) is a solution of the operator equation Lx=λNx. Then, there exist the positive constants ρk,dk, and δk such that the following inequalities
0<ln(δk)<xk(t)<ln(ρkω)+dk,k=¯1,6, | (3.10) |
are satisfied for t∈[0,ω].
Proof. The proof is constructive. First we find the definition of the constant δk, and subsequently the constants ρkand dk. In order to obtain δk, we arbitrarily chose x∈Dom(L) such that Lx=λNx. By multiplying each equation of the system (Lx)T(t)=λ(Nx)T(t) and rearranging the result appropriately, we deduce the following:
dex1dt+[λβ(t)ex6]ex1=λγ(t)ex3>0, | (3.11) |
dex2dt+λα(t)ex2=λβ(t)ex6+x1>0, | (3.12) |
dex3dt+λγ(t)ex3=λα(t)ex2>0, | (3.13) |
dex4dt+[λ(μ1(t)+μ2(t)P(ex4+ex5+ex6))+λν(t)ex3]ex4=λΛ(t)(ex4+ex5+ex6)+λκex6>0, | (3.14) |
dex5dt+[λ(μ1(t)+μ2(t)P(ex4+ex5+ex6))+λθ(t)]ex5=λν(t)ex3+x4>0, | (3.15) |
dex6dt+[λ(μ1(t)+μ2(t)P(ex4+ex5+ex6))+λκ(t)]ex6=λθ(t)ex5>0. | (3.16) |
From the estimates in (3.3) and the assumptions of Theorem 1.1, we have the following inequalities
0<mint∈[0,ω][λ(μ(t)+μ2(t)PV__)+λθ(t)]≤λ(μ1(t)+μ2(t)P(ex4+ex5+ex6))+λθ(t)≤‖μ1‖∞+‖μ2‖∞P¯¯V+‖θ‖∞,t∈[0,ω],0<mint∈[0,ω][λ(μ1(t)μ2(t)PV__)+λκ(t)]≤λ(μ1(t)+μ2(t)P(ex4+ex5+ex6))+λκ(t)≤‖μ1‖∞+‖μ2‖∞P¯¯V+‖κ‖∞,t∈[0,ω]. |
By using the fact that ex5(0)=V0e/P and ex6(0)=V0i/P, and applying Proposition 3.2 to (3.15) and (3.16), we deduce the following estimates:
ex5(t)≥V0ePexp(−[‖μ1‖∞+‖μ2‖∞P¯¯V+‖θ‖∞]ω):=δ5,t∈[0,ω], | (3.17) |
ex6(t)≥V0iPexp(−[‖μ1‖∞+‖μ2‖∞P¯¯V+‖κ‖∞]ω):=δ6,t∈[0,ω]. | (3.18) |
We notice that (3.3) and (3.18) imply the following inequalities:
0<mint∈[0,ω][λβ(t)]δ6≤λβ(t)ex6(t)≤‖β‖∞¯¯V,t∈[0,ω],0<λmint∈[0,ω]α(t)≤λα(t)≤‖α‖∞,t∈[0,ω],0<λmint∈[0,ω]γ(t)≤λγ(t)≤‖γ‖∞,t∈[0,ω]. |
Then, the application of Proposition 3.2 to (3.11), (3.12), and (3.13) implies the following:
ex1(t)>ex1(0)exp(−‖β‖∞¯¯Vω)=P0sPexp(−‖β‖∞¯¯Vω):=δ1,t∈[0,ω], | (3.19) |
ex2(t)>ex2(0)exp(−‖α‖∞ω)=P0ePexp(−‖α‖∞ω):=δ2,t∈[0,ω], | (3.20) |
ex3(t)>ex3(0)exp(−‖γ‖∞ω)=P0iPexp(−‖γ‖∞¯¯Vω):=δ3,t∈[0,ω]. | (3.21) |
Similarly, from (3.3) and (3.21), we deduce the following:
0<mint∈[0,ω][λ(μ1(t)+μ2(t)PV__)+λν(t)δ3]≤λ[μ1(t)+μ2(t)P(ex4(t)+ex5(t)+ex6(t))]+λν(t)ex3(t)≤‖μ1‖∞+‖μ2‖∞P¯¯V+‖ν‖∞,t∈[0,ω], |
and by the initial condition ex4(0)=V0s/P and Proposition 3.2, we obtain the following:
ex4(t)>V0sPexp(−‖β‖∞[‖μ1‖∞+‖μ2‖∞P¯¯V+‖ν‖∞]ω):=δ4,t∈[0,ω]. | (3.22) |
The relations (3.17)–(3.22) prove the following estimate:
0<ln(δk)<xk(t),k=1,…,6,t∈[0,ω]. | (3.23) |
The construction of ρk for any x∈Dom(L) which satisfies the operator equation Lx=λNx can be developed as follows. From Proposition 3.1, we deduce that the following:
0<∫ω0(exk)dt≤∫ω0(ex1(t)+ex2(t)+ex3(t))dt=∫ω0dt=ω:=ρk, k = 1,2,3 , | (3.24) |
0<∫ω0(exℓ)dt≤∫ω0(ex4(t)+ex5(t)+ex6(t))dt=∫ω0¯¯Vdt=¯¯Vω:=ρℓ,ℓ=4,5,6. | (3.25) |
Applying the Mean Value Theorem for integrals to the function exk for k=1,…,6 over [0,ω], we follow that there exists ξk∈[0,ω] such that exk(ξk)=ω−1∫ω0exkdt, and consequently
there exists ξk∈[0,ω] such that xk(ξk)=ln(ρkω),k=1,…,6. | (3.26) |
Integrating the system (Lx)T(t)=λ(Nx)T(t) over [0,ω] and the ω−periodic behavior of x, we obtain the following:
∫ω0λ(−βex6+γex3−x1)dt=0,∫ω0λ(βex1+x6−x2−α)dt=0,∫ω0λ(αex2−x3−γ)dt=0,∫ω0λ(Λ(ex4+ex5+ex6)e−x4−(μ1+μ2P(ex4+ex5+ex6))−ν(t)ex3+κ(t)ex6−x4)dt=0,∫ω0λ(−(μ1+μ2P(ex4+ex5+ex6))+νex3+x4−x5−θ(t))dt=0,∫ω0λ(−(μ1+μ2P(ex4+ex5+ex6))+θ(t)ex5−x6−κ(t))dt=0, |
which implies that
∫ω0e(x3−x1)(t)dt≤‖β‖∞¯¯Vωmint∈[0,ω]γ(t),∫ω0e(x1+x6−x2)(t)dt≤‖α‖∞ωmint∈[0,ω]β(t),∫ω0e(x2−x3)(t)dt≤‖γ‖∞ωmint∈[0,ω]α(t),∫ω0e−x4(t)dt≤(‖μ1‖∞+‖μ2‖∞P¯¯V+‖ν‖∞)ωV__mint∈[0,ω]Λ(t),∫ω0e(x6−x4)(t)dt≤(‖μ1‖∞+‖μ2‖∞P¯¯V+‖ν‖∞)ωmint∈[0,ω]κ(t),∫ω0e(x4+x3−x5)(t)dt≤(‖μ1‖∞+‖μ2‖∞P¯¯V+‖θ‖∞)ωmint∈[0,ω]ν(t),∫ω0e(x5−x6)(t)dt≤(‖μ1‖∞+‖μ2‖∞P¯¯V+‖κ‖∞)ωmint∈[0,ω]θ(t). |
Then, taking the absolute value of the system (Lx)T(t)=λ(Nx)T(t) and integrating over [0,ω], we obtain the following upper bounds:
∫ω0|dx1dt|dt≤∫ω0(βex6+γex3−x1)(t)dt≤‖β‖∞¯¯Vω(1+‖γ‖∞mint∈[0,ω]γ(t)):=d1, | (3.27) |
∫ω0|dx2dt|dt≤∫ω0(βex6+x1+x2+α)(t)dt≤‖α‖∞ω(1+‖β‖∞mint∈[0,ω]β(t)):=d2, | (3.28) |
∫ω0|dx3dt|dt≤∫ω0(αex2−x3+γ)(t)dt≤‖γ‖∞ω(1+‖α‖∞mint∈[0,ω]α(t)):=d3, | (3.29) |
∫ω0|dx4dt|dt≤∫ω0[Λ(ex4+ex5+ex6)e−x4+(μ1+μ2P(ex4+ex5+ex6))+νex3+κex6−x4](t)dt≤ω(‖μ1‖∞+‖μ2‖∞P¯¯V+‖ν‖∞)(1+¯¯V‖Λ‖∞V__mint∈[0,ω]Λ(t)+‖κ‖∞mint∈[0,ω]κ(t)):=d4, | (3.30) |
∫ω0|dx5dt|dt≤∫ω0[(μ1+μ2P(ex4+ex5+ex6))+νex4+x3−x5+θ](t)dt≤ω(‖μ1‖∞+‖μ2‖∞P¯¯V+‖θ‖∞)(1+‖ν‖∞mint∈[0,ω]ν(t)):=d5, | (3.31) |
∫ω0|dx6dt|dt≤∫ω0[(μ1+μ2P(ex4+ex5+ex6))+θex5−x6+κ](t)dt≤ω(‖μ1‖∞+‖μ2‖∞P¯¯V+‖κ‖∞)ω(1+‖θ‖∞mint∈[0,ω]θ(t)):=d6. | (3.32) |
To complete the proof, we note ∫tξkx′k(τ)dτ=xk(t)−xk(ξk) for k=1,…,6. Then, from (3.26) and (3.27)–(3.32), we have the following:
xk(t)=xk(ξk)+∫tξkdxk(τ)dτdτ≤xk(ξk)+∫ω0|dxk(τ)dτ|dτ≤ln(ρkω)+dk,k=1,…,6,t∈[0,ω]. | (3.33) |
Hence, by the estimates (3.23) and (3.33), we deduce (3.10) and conclude the proof of the lemma.
Lemma 3.2. Assume that the hypotheses of Lemma 3.1 are satisfied. If x∈Ker(L) is a solution of the operator equation QN(x)=0, then there exist positive constants ρk and δk such that the inequality
0<ln(δk)<xk(t)<ln(ρkω),k=1,…,6, | (3.34) |
is satisfied for t∈[0,ω].
Proof. From Lemma 2.1, it follows that Ker(L)≅R6, which implies that x∈Ker(L) is equivalent to x=c, where c is a constant vector. Assume the hypothesis that x satisfies the operator equation QN(x)=0, or equivalently QN(c)=0. From the definition of Q, we follow that
QN(c)=0⇔1ω∫ω0N(c)dτ=0⇔N(c)=0=L(c). |
Then, for any λ∈(0,1), it follows that λN(c)=0=L(c) and consequently λN(c)=L(c). Then, by similar arguments to the proof of Lemma 3.1, we deduce there exist δk,ρk and dk=0 for k=1,…,6 such that the estimate (3.34) is satisfied.
Lemma 3.3. Let X=Y=F with F, the Banach spaces are defined in (1.8); Ω⊂F, the open ball centred at 0 and radius h, with h defined as follows:
h=max{6∑k=1ln(δk);6∑k=1(ln(ρkω)+dk)} | (3.35) |
where δk,ρk, and dk are as defined in (3.19) and (3.20), (3.24) and (3.25), and (3.27)–(3.32), respectively. Then, the items (C1), (C2), and (C3) of Theorem 2.1 are satisfied.
Proof. The proof of (C1) will be developed by contradiction. We begin by considering that the statement is false, or equivalently we consider that there exists (λ,x)∈(0,1)×[∂Ω∩Dom(L)] such that L(x)=λN(x). Then, by the application of Lemma 3.1, we follow that 0<ln(δk)<xk(t)<ln(ρk/ω)+dk for k=1,…,6, which implies the following:
6∑k=1ln(δk)<6∑k=1xk(t)<6∑k=1(ln(ρkω)+dk),t∈[0,ω]. | (3.36) |
Using the definition of h given on (3.35), we have that that h can reduced to the following relation:
h=max{6∑k=1ln(δk);6∑k=1(ln(ρkω)+dk)}=6∑k=1(ln(ρkω)+dk). |
We notice that (3.36) implies the relation ‖x‖<h, or equivalently x belongs to the interior of Ω, which is a contradiction, since we have assumed that x∈∂Ω.
To prove (C2), we also apply a contradiction argument. If (C2) is false, then we can find x∈Ker(L)∩∂Ω, such that QN(x)=0. Then, by Lemma (3.2), we follow that 0<ln(δk)<xk(t)<ln(ρk/ω) for k=1,…,6, and consequently
h=max{6∑k=1ln(δk);6∑k=1ln(ρk)}=6∑k=1ln(ρkω)and‖x‖<h. |
Here, x∈Ω is a contradiction, since we have considered that x∈Ker(L)∩∂Ω. Then, (C2) is satisfied.
In order to prove (C3), we consider x∈Dom(L) and ε∈[0,1], and define the homotopy H:Dom(L)×[0,1]→E, by the following relation:
H(x,ε)=(−¯βex6+¯γ¯βex6+x1−x2−¯α¯αex2−x3−¯γ¯κex6−x4−¯μ1¯νex4+x3−x5−(¯μ1+¯θ)¯θex5−x6−(¯μ1+¯κ))T+ε(¯γ(ex3−x1−1)00¯Λ(ex4+ex5+ex6)e−x4−¯μ2P(ex4+ex5+ex6)−¯νex3−¯μ2P(ex4+ex5+ex6)−¯μ2P(ex4+ex5+ex6))T, |
where
(¯β,¯α,¯γ,¯κ,¯ν,¯θ,¯Λ,¯μ1,¯μ2)=1ω∫ω0(β,α,γ,κ,ν,θ,Λ,μ1,μ2)(t)dt. |
We claim the following:
If x∈Ker(L)∩∂Ω and ε∈[0,1], then H(x,ε)≠0. | (3.37) |
Indeed, suppose that there exists x∈Ker(L)∩∂Ω and ε∈[0,1] such that H(x,ε)=0. Since Ker(L)≅R6, we have that x(t)=x(0) and H(x,ε)=H(x(0),ε)=0. Therefore, from the definition of H,
0=−¯βex6(0)+¯γ+ε¯γ(ex3−x1−1)0=¯βe(x1+x6−x2)(0)−¯α,0=¯αe(x2−x3)(0)−¯γ,0=¯κe(x6−x4)(0)−¯μ1+ε[¯Λ(ex4(0)+ex5(0)+ex6(0))e−x4(0)−¯μ2P(ex4(0)+ex5(0)+ex6(0))−¯νex3(0)],0=¯νe(x3+x4−x5)(0)−(¯μ1+¯θ)−ε¯μ2P(ex4(0)+ex5(0)+ex6(0)),0=¯θe(x5−x6)(0)−(¯μ1+¯κ)−ε¯μ2P(ex4(0)+ex5(0)+ex6(0)). |
Proceeding analogously to the proof of Lemma 3.1, we can deduce that ‖x(0)‖<h, or equivalently x(t)=x(0)∈Ω, which is a contradiction with the assumption that x∈∂Ω. Hence, the claim (3.37) is verified.
On the other hand, it is known that there exists an isomorphism J:Ker(L)→Im(Q), which implies that Ker(L)≅Im(Q). Then, without a loss of generality, we can choose J=I. It follows that: JQN=IQN=QN and deg(JQN(x),Ker(L)∩Ω,0)=deg(QN(x),Ker(L)∩Ω,0). Then, from (3.37), we can use the homotopy invariance property of the degree of coincidence to obtain the following:
deg(QN(x),Ker(L)∩Ω,0)=deg(H(x,1),Ker(L)∩Ω,0)=deg(H(x,0),Ker(L)∩Ω,0). |
Using the facts that
H(x,0)=(−¯βex6+¯γ,¯βex1+x6−x2−¯α,¯αex2−x3−¯γ,¯κex6−x4−¯μ1,¯νex3+x4−x5−(¯μ1+¯θ),¯θex5−x6−(¯μ1+¯κ)), |
and the algebraic system H(x,0)=0, i.e.,
0=−¯βex6+¯γ,0=¯βex1+x6−x2−¯α,0=¯αex2−x3−¯γ,0=¯κex6−x4−¯μ1,0=¯νex3+x4−x5−(¯μ1+¯θ),0=¯θex5−x6−(¯μ1+¯κ), |
has a unique solution x∗∈∂Ω∩Ker(L), we deduce the following:
deg(H(x,0),Ker(L)∩Ω,0)=sgn(|∂x1H1(x∗,0)∂x2H1(x∗,0)∂x3H1(x∗,0)∂x4H1(x∗,0)∂x5H1(x∗,0)∂x6H1(x∗,0)∂x1H2(x∗,0)∂x2H2(x∗,0)∂x3H2(x∗,0)∂x4H2(x∗,0)∂x5H2(x∗,0)∂x6H2(x∗,0)∂x1H3(x∗,0)∂x2H3(x∗,0)∂x3H3(x∗,0)∂x4H3(x∗,0)∂x5H3(x∗,0)∂x6H3(x∗,0)∂x1H4(x∗,0)∂x2H4(x∗,0)∂x3H4(x∗,0)∂x4H4(x∗,0)∂x5H4(x∗,0)∂x6H4(x∗,0)∂x1H5(x∗,0)∂x2H5(x∗,0)∂x3H5(x∗,0)∂x4H5(x∗,0)∂x5H5(x∗,0)∂x6H5(x∗,0)∂x1H6(x∗,0)∂x2H6(x∗,0)∂x3H6(x∗,0)∂x4H6(x∗,0)∂x5H6(x∗,0)∂x6H6(x∗,0)|)=sgn(|00000−¯βex∗6¯βex∗1+x∗6−x∗2−¯βex∗1+x∗6−x∗2000¯βex∗1+x∗6−x∗20¯αex∗2−x∗3−¯αex∗2−x∗3000000−¯κex∗6−x∗40¯κex∗6−x∗400¯νex∗3+x∗4−x∗5¯νex∗3+x∗4−x∗5−¯νex∗3+x∗4−x∗500000¯θex∗5−x∗6−¯θex∗5−x∗6|)=sgn(2¯β2¯α¯κ¯ν¯θex∗1+2x∗6)=1. |
Then, deg(JQN,Ω∩Ker(L),0)=1≠0. In this way, condition the item (C3) of Theorem 2.1 is verified.
The existence of the solution for Lx=Nx on Dom(L)∩¯Ω is a straightforward consequence of the application of Theorem 2.1 since the items (C1), (C2), and (C3) are satisfied.
We can rewrite the system (1.1)–(1.7) as the operator equation of the form (1.11) (see Theorem A.1) on E with the operators L and N defined in (1.9) and (1.10), respectively. Moreover, the items (C1), (C2), and (C3) of Theorem 2.1 are satisfied by Lemma 3..3. Hence, by application of Theorem 2.1 there exists at least one solution of the operator equation Lx=Nx on Dom(L)∩¯Ω with Ω defined on (1.13) and σ=h (see (3.35)). Moreover, from the change of variable (1.12), we obtain the existence (Ps,Pe,Pi,Vs,Ve,Vi)T(t), which is a positive periodic solution of (1.1)–(1.7).
In this section, the objective is to provide a general proof of concept that the governing equations can qualitatively resemble expected population dynamics, without specific adjustments for a quantitative calibration. The biological considerations related to the flavescence dorée (see, e.g., [45,46]) serve as a general reference for the model.
The population sizes are non-dimensional, where "1" corresponds to a reference unit; the initial values are adjusted such that the corresponding species (plant or vector) sum up to "1". The time scales are adjusted to reflect the realistic scenarios of the typical life cycles based on the temporal dynamics of the following species:
● Grapevines (Vitis spp.): Grapevines are perennial plants with no specific lifespan; they can live for many years if kept healthy. Commercial vineyards typically replace grapevines after 25–30 years, as the fruit production may decline by then. Therefore, 10,000 days, which corresponds to approximately 27.4 years, can be considered a the reference timespan; for the simulations, we chose 1000 days as a the time span, which allows us to visualize three cycles.
● Flavescence dorée: This disease is caused by phytoplasma, which is a bacterium without cell walls. The phytoplasma reproduces by binary fission within the phloem of a host plant. The phloem is a tissue in vascular plants that transports soluble organic compounds from the leaves to other parts of the plant. The phytoplasma relies entirely on the grapevine for survival and reproduction and spreads to other plants only through insect vectors, such as leafhoppers.
● Scaphoideus titanus (leafhopper): This insect has one generation per year, with life cycle stages varying based on the hemisphere:
– Eggs are laid in late summer (August-October in the Northern Hemisphere; February-May in the Southern Hemisphere) and over winter on the vine.
– Nymphs hatch in late spring, typically around mid-May (Northern Hemisphere) or mid-November (Southern Hemisphere) of the following year.
– Adults emerge from the final nymphal stage in mid-summer (June-July in the Northern Hemisphere; December-January in the Southern Hemisphere). During this time, they can acquire and transmit the flavescence dorée phytoplasma while feeding on the grapevine sap. Adults live for 1–3 months, dying in late summer.
For Example 1, the following parameter specifications are chosen:
● The life span of the vector is set to μ−11=20 days, which corresponds to a natural mortality rate of μ1=0.05 (per day).
● The density-dependent mortality rate is specified as μ2=0.001 (per day per vector).
● For the recruitment rate, Λ, we estimate an average lifetime fecundity of approximately 30–40 eggs per female. This estimate is based on 2–4 clutches per female during their adult life, with each clutch containing 5–20 eggs. While technically not a pregnancy, but rather oviposition, the females lay eggs either singly or in small clutches within the plant tissues after mating. As a result, we estimate an egg-laying rate between 0.01 and 0.06 eggs per day, with 0.06 being an optimistic estimate and 0.01 being a more conservative rate, thereby accounting for lower egg survival rates. In the examples, the main variations operate on changes of Λ.
● The probability of transmission of the bacterium from the plant to the vector, denoted by β, is estimated at 0.1, or 10%. This value lies within a reasonable range of 2–40%.
● Similarly, the probability of transmission of the bacterium to the grapevine, denoted by ν, is also estimated at ν=0.1, which falls within the 2–40% range, thus representing the probability that the susceptible vectors become infected within a unit of time.
● The parameter θ−1 represents the average incubation period of the bacterium in the vector. Although the bacterium slowly multiplies within the vector after ingestion, we assume an incubation period of 30 days, which corresponds to θ=1/30≈0.033. This value is adopted according to [30] (see also [47]): "An incubation period of about 1 month, during which time the phytoplasma multiplies and colonizes the vector's body, is required before the vector becomes infectious."
● The parameter α−1 denotes the average incubation time of the bacterium in the grapevine. Flavescence dorée, caused by phytoplasmas, typically has an incubation period of one year or more before symptoms manifest on the grapevine. This prolonged period allows the phytoplasma to reproduce and overcome the plant defenses. We set α−1=365, meaning α=1/365≈0.0027.
● The recovery parameter is set to κ=0, as no recovery occurs in the case of flavescence dorée. Once the vector (leafhopper) acquires the infection, it becomes systemic, meaning the vector remains infectious for the rest of its life, with no possibility of recovery. This corresponds to an infinite average recovery time of the vector κ−1.
● The parameter γ−1 represents the average time the grapevine remains infectious. A grapevine infected with flavescence dorée remains infectious for its entire lifespan due to the systemic nature of the infection, which affects the entire vascular system of the vine. Hence, we set γ=0, as the infection persists indefinitely, with no recovery or reduction in the infectivity.
The initial condition
x(0)=x0=(0.8,0.15,0.05,0.7,0.2,0.1), | (5.1) |
is adjusted such that the fractions of each species (plants or vectors) adds to 1, thus providing a dominance of susceptible species. The initial values of each variable are intentionally chosen to create a visual distinction between the functions. In Examples 1(a)–(c), we select the following variations of the constant function Λ(t): {0.04,0.05,0.06}. See Figure 2 for a visualization of the simulation across all variables.
The plot employs a logarithmic scale on the x-axis to capture the long-term behavior and the asymptotic trends of the plant variables Pe and Pi within the range [100,1000], while still adequately visualizing the short-term behavior of the vector variables in the range [0,100].
In Figure 2(a), for Λ(t)≡0.04, all vector populations monotonically decrease and eventually vanish. This outcome is expected for smaller recruitment rates Λ(t). The infected plant population monotonically increases towards an asymptotic value, while the susceptible plant population monotonically decreases, appearing to approach a non-zero asymptotic value. This non-zero value results from the absence of the vector populations, which would otherwise drive the susceptible plant population further down. The exposed plant population initially increases to a maximum and then declines to an asymptotic value of zero.
How do these dynamics change with an increase in the recruitment rate? This can be seen in Figure 2(b), where Λ(t)≡0.05. When the recruitment rate increases, the vector populations, particularly the infected vector Vi, which does not vanish as in the previous example, but can stabilize at a non-zero level.The susceptible vectors Vs initially increase, reach a maximum, and then begin to decline. From the visualization, it is unclear whether the asymptotic value of Vs is zero; however, based on the equations, it should eventually converge to zero. The other two vector populations, Ve and Vi, first decrease, reaching a minimum (first Ve, followed by Vi), and then increase towards an asymptotic state. Additionally, the dynamics of the plant population change: in contrast to the previous example, the susceptible plant population Ps quickly vanishes within the overall time interval.
In Example 1(c), the recruitment rate is further increased to Λ(t)≡0.06, thus leading to an uncontrolled rise in all vector populations, as illustrated in Figure 2(c). The qualitative behavior of the plant population remains the same, with the notable difference being that the exposed plant population Pe exhibits a more pronounced peak.
In Example 2, we want to explore the effect of periodic parameters by modifying the equation that governs the susceptible vector population, Vs. The goal of this adjustment is to control the growth of the vector population. The modified equation for Vs is as follows:
dVs(t)dt=Λ(t)−(μ1(t)+μ2(t)⋅V(t))Vs(t)−ν(t)Vs(t), |
where we replace the term Λ(t)V with Λ(t), which is now defined by the following:
Λ(t)=λ1(t)+λ2(t)V. |
This modification offers a significant advantage: it makes the growth rate of Vs independent of the total vector population V. In cases where the vector population V drastically decreases, the growth of Vs is no longer tightly coupled to V, thus preventing a prolonged delay in recovery.
Then, the governing equation for Vs(t) is then slightly modified:
dVs(t)dt=Λ(t)−(μ1(t)+μ2(t)∗V(t))Vs(t)−ν(t)Vs(t)Pi(t)+κ(t)Vi(t). |
In this second example, the same initial conditions are used as in Example 1, along with most of the same parameters. The primary difference is the modification of Λ(t), which is chosen as the following periodic function:
Λ(t)={λ1if (tmod365)<60,0otherwise. | (5.2) |
Here, Λ(t) is defined as active for 60 days each year (representing a seasonal factor, such as increased vector reproduction during specific months). For Example 2(a), we set λ1=0.02, and we increase λ1 to 0.04 for Example 2(b) to simulate a higher vector birth rate during the active period.
Figures 3 and 4 depict the simulations for Examples 2(a) and 2(b), respectively. These simulations illustrate the periodic behavior of the plant and vector populations over time, with varying levels of periodicity in the vector growth rate, which is controlled by the different values of λ1.
This example demonstrates how altering the periodicity and the vector population's growth rate affects the plant-vector system's overall dynamics. By tuning parameters such as λ1, vineyard managers or researchers could explore different scenarios, such as varying climatic conditions or vector control interventions.
The dynamics of the vector population are primarily driven by their recruitment rate, Λ, which is considered as a primary control variable, and focused on in this second example. During a typical season, the susceptible vector population Vs initially increases, thus approaching its upper carrying capacity, which exceeds the eventual peaks of the other vector stages. As this happens, the exposed vector population Ve rises and eventually overtakes the susceptible population.
The effect of the halt in growth is immediate: a steep drop in Vs triggers a more moderate decline in Ve, thus leading to a gradual decrease in Vi. Similarly, a decrease in Ps causes a slight increase in Pe. When the growth is stopped (i.e., when Λ=0), the susceptible population populations experience a sharp decline, immediately followed by the exposed population. This anticipates the end of the adult generation. Simultaneously, the infected population reaches its peak, and then decreases. This timing is significant: the infected population peaks just as the birth rate halts. After this point, all vector populations decline to minimal levels, thus eventually disappearing. The dynamics of the plant populations mirror those of the vector populations.
The dynamics of the plant populations mirror those of the vector populations. When the infected vectors are present – typically following a bell-shaped curve with a kink at the peak – the susceptible plant population decreases in an inverse S-shaped pattern. Conversely, when the infected vectors are absent, the number of susceptible plants remains stable.
Interestingly, the number of exposed plants decreases during periods of low vector load and slightly increases during a stronger vector presence. This decrease may seem counterintuitive: why should the plant populations change when the vectors are absent? Without a significant vector population, one would expect little change in the plant populations. However, if the exposed plants are present, then they will convert into infected plants according to the system's dynamics. In this example, we chose a relatively high initial number of exposed plants. While this higher initial value might not represent a typical real-world case, it is included here for didactic purposes to examine the behavior of the system's equations.
The increasing number of infected plants is expected, as the process is designed to be irreversible – no plant recovery is considered. A key observation is that the rate of increase in the infected plants does not noticeably change during the period of vector emergence. This didactic example is due to the relatively high number of exposed plants, which dampens any significant change in the overall percentage of infected plants.
Our model for the recruitment rate assumed that births do not occur continuously throughout the year, but are seasonally concentrated. This can be modeled using a seasonally varying function that peaks during the leafhopper's breeding season. In our model, we chose a piecewise constant function that took a positive value during the breeding season and dropped to zero outside of it. This approach is both practical and effective in the absence of detailed data. While alternative functional forms could be considered, the key factors to capture are the average length of the breeding season and the breeding intensity.
In this paragraph, some potential improvements to the model are discussed.
As leafhoppers progress through different life stages (eggs, nymphs, adults), these stages could be modeled with distinct variables to gain a quantitative control over their development. This distinction is reasonable since only adults can infect plants, while the other stages are crucial for tracking the effective number of future adults in the next generation. Of particular relevance are the nymph dynamics, as pathogen acquisition can occur during both the nymph and adult stages.
To better capture the leafhopper life cycle, we could introduce two key state variables: N for eggs/nymphs, which represents a latent period, and V∗ for adults, which represents an active period that involves both reproduction and infection. Then, the model equations could be modified as follows:
˙N=λV−σN+…˙Vs=σN+… |
In the first equation, the term λV accounts for the creation of new eggs/nymphs, and the term σN represents the transition of nymphs to adults. In the second equation, the corresponding −σN term accounts for the removal of nymphs as they transition to adults. The function σ could vary seasonally (e.g., with σ=0 during the breeding season and σ>0 during hatching).
It also might be useful to formally classify two levels of infection within the plants:
1) The overall statistics of the plant population, which indicates the percentage of plants in each infection status (i.e., whether a plant is infected or not, without specifying the severity of infection).
2) The degree of infection within an individual plant, thus acknowledging that the extent of bacterial growth within a plant influences the probability of transmission.
This distinction is valuable because the severity of infection within the individual plants can significantly affect the overall dynamics of disease spread.
The findings of this study have important real-world implications for disease management and prevention in vineyards, particularly in controlling flavescence dorée. By incorporating seasonality and periodic dynamics into the mathematical model, vineyard managers can better predict the timing and intensity of disease outbreaks, thus allowing for more precise interventions. For instance, the identification of key periods when the vector population is likely to surge or when grapevines are most vulnerable to infection can inform the timing of pesticide applications, thus reducing the need for constant chemical use and lowering environmental impact. Additionally, the model's ability to simulate various control strategies—such as vector population reduction, quarantine measures, or the introduction of disease-resistant grapevines—provides vineyard managers with valuable tools to assess the effectiveness of these approaches before implementation. This leads to more sustainable and cost-effective practices, as well as better long-term vineyard health, thereby reducing crop losses and increasing productivity. Ultimately, the integration of such modeling into disease management programs enhances the decision-making processes, thus aligning with the broader goals of sustainable agriculture.
A. Coronel, F. Huancas: Supervision; A. Coronel, F. Huancas, R. Vidal: Methodology, Writing-original draft, Visualization; A. Coronel, F. Huancas, R. Vidal, S. Berres, H. Brito: Conceptualization, Formal analysis, Investigation, Writing-review & editing; A. Coronel, F. Huancas, S. Berres: Funding acquisition. All authors have read and agreed to the published version of the manuscript.
The authors declare they have not used Artificial Intelligence (AI) tools in the creation of this article. However, the authors declare to have used as Artificial Intelligence (AI) tools, namely ChatGPT for cross-checking and specifically for improving the grammar throughout the paper.
This work is partially supported by the Agencia Nacional de Investigación y Desarrollo, ANID-Chile, through the project FONDECYT 1230560 and by the Universidad Tecnológica Metropolitana through the program Proyectos Regulares de Investigación, año 2023, código LPR23-03.
The authors declare that they have no conflict of interest.
Theorem A.1. Consider that the hypothesis of Theorem 1.1 are satisfied. Let L and N be the operators defined in (1.9) and (1.10), Respectively, and consider x(t)=(x1,…,x6)T(t) defined by (1.12). Then, the following statements are true:
(a) x is a solution of the operator equation (1.11) if and only if a solution of (Ps,Pe,PI,Vs,Ve,Vi) is a solution of the system (1.1)–(1.7).
(b) If the solution of (1.11) is ω−periodic, then the solution of system (1.1)–(1.7) is also ω−periodic.
(c) If operator equation (1.11) has a solution. Then system (1.1)–(1.7) has a positive solution.
Proof. In order to prove Theorem A.1-(a), we begin by noticing that the change of variable (1.12) and differentiation imply the following identities:
ddtx(t)=1P(e−x1(t)dPsdt,e−x2(t)dPedt,e−x3(t)dPidt,e−x4(t)dVsdt,e−x5(t)dVedt,e−x6(t)dVidt)(t), | (A.1) |
ddt(Ps,Pe,Pi,Vs,Ve,Vi)=(Pex1dx1dt,Pex2dx2dt,Pex3dx3dt,Pex4dx4dt,Pex5dx5dt,Pex6dx6dt). | (A.2) |
If (Ps,Pe,Pi,Vs,Ve,Vi)T is a solution of system (1.1)–(1.7), then using (A.1) and (1.12), we deduce that x is a solution of the following system:
dx1dt=−β(t)ex6+γex3−x1, | (A.3) |
dx2dt=β(t)ex6+x1+x2−α, | (A.4) |
dx3dt=αex2−x3−γ, | (A.5) |
dx4dt=Λ(t)(ex4+ex5+ex6)e−x4−(μ1+μ2P(ex4+ex5+ex6))−ν(t)ex3+κex6−x4, | (A.6) |
dx5dt=−(μ1+μ2P(ex4+ex5+ex6))+ν(t)ex4+x3−x5−θ, | (A.7) |
dx6dt=−(μ1+μ2P(ex4+ex5+ex6))+θex5−x6−κ, | (A.8) |
x(0)=(ln(P0sP),ln(P0eP),ln(P0iP),ln(V0sP),ln(V0eP),ln(V0iP)). | (A.9) |
Using the operators L and N defined in (1.9) and (1.10), respectively, we can rewrite the system (A.3)–(A.9) as the operator equation (1.11). Conversely, if we consider that x satisfies (1.11), we deduce that x is a solution of (A.3)–(A.9); then by the application of (A.2) and (1.12), we get that (Ps,Pe,Pi,Vs,Ve,Vi)T is a solution of system (1.1)–(1.7).
The proofs of items (b) and (c) of Theorem A.1 are straightforward consequence of (1.12).
(a) Let x∈Ker(L), (i.e., L(x)=0∈R6). Then, by the definition of the operator L, we deduce that x′(t)=0, or equivalently that x(t)=x(0) for t∈[0,ω]. Thus, we deduce that Ker(L)≅R6 and dim(Ker(L))=6<∞. Applying the elementary algebra results, we obtain the following: (ⅰ) X≅Ker(L)⨁(X/Ker(L)); (ⅱ) Y≅Im(L)⨁(X/Ker(L))≅Im(L)⨁(Y/Ker(L)), since X=Y; and (ⅲ) Im(L)≅(X/Ker(L)). Using (ⅲ) in (ⅰ), it follows that X≅Ker(L)⨁(X/Ker(L))≅Ker(L)⨁Im(L); and from (ⅱ), Y≅(Y/Ker(L))⨁Im(L), which implies that Ker(L)≅(Y/Ker(L)) using the fact that X=Y. Therefore, dim(Ker(L))=dim(Y/Ker(L))=codim(Im(L))=6<∞.
In order to prove that Im(L) is a closed set, we select arbitrarily y∈Im(L). Then, we can find x∈Dom(L) such that L(x)=y, and by the definition of L and the fact that x∈X, we deduce the following
L(x)=y⇔dx(t)dt=y(t)⇔∫t+ωtdx=∫t+ωty(τ)dτ⇔0=∫t+ωty(τ)dτ. |
Equivalently, Im(L) is characterized by Im(L)={y∈Y:∫ω0y(τ)dτ=0}. Moreover, it follows that for a continuous f:Im(L)⊂X→R6; f−1(0T)=Im(L) is a closed set; because {0T} is a closed set of R6.
Hence, we have that L is a Fredholm operator of index zero.
(b) Consider the sequence {xn}⊂X and ¯x∈X such that xn→¯x in the topology induced by the norm of X. Based on the definition of the operator N as given in (1.10), and applying the inequality component-wise,
|exp(z2)−exp(z1)|=|∫z1z2exp(s)ds|≤max{exp(z1),exp(z2)}|z2−z1|,∀z1,z2∈R, |
we establish the existence of a constant C>0 depending only on ψ, ϕ, ν, θ, α, β, γ, and κ, such that ‖N(xn)−N(¯x)‖≤C‖xn−¯x‖. This leads to the conclusion that N(xn)→N(¯x) in the norm of E, proving that N is continuous.
(c) By the definition of the operator P, we easily deduce that it is linear, continuous, and is a projector, since
P2(x)=P(P(x))=P(1ω∫ω0x(τ)dτ)=1ω∫ω01ω∫ω0x(τ)dτds=1ω∫ω0ds⋅1ω∫ω0x(τ)dτ=ωω1ω∫ω0x(τ)dτ=1ω∫ω0x(τ)dτ=P(x). |
Using the fact that P=Q, we have the same conclusions for the operator Q (i.e., Q is linear, continuos and is a projector).
We prove that Ker(L)=Im(P) by using the double inclusion argument. We can deduce that Ker(L)⊂Im(P); by the results of Lemma 2.1–(a), we can apply the following arguments: if x∈Ker(L)≅R6, then we have that x(t) is a constant function on [0,ω], then P(x)=x or equivalently x∈Im(P). Conversely, we prove that Im(P)⊂Ker(L) as follows: if y∈Ker(L), then there exists z∈X such that P(z)=y; and from the definition of P, we get ω−1∫ω0z(τ)dτ=y, i.e., L(y)=0, which implies that y∈Ker(L).
We prove that Ker(Q)=Im(L) using the definition of the operator Q and the characterization of Im(L) given on the item (a): y∈Ker(Q) is equivalent to ∫ω0y(τ)dτ=0 or y∈Im(L). To prove Im(I−Q)=Im(L), we consider y∈Im(I−Q); then, there exists z∈X such that
(I−Q)(z)=y⇔∫ω0(z(τ)−1ω∫ω0z(m)dm)dτ=∫ω0y(τ)dτ=0⇔y(τ)∈Im(L). |
The last equivalence is obtained by the application of item (a). Hence, we deduce that Im(I−Q)=Im(L).
Let us prove the existence of the Operators KP and LP. The operator LP is the restriction of L to Dom(L)∩Ker(P) (i.e., LP:Dom(L)∩Ker(P)→Im(L) and LP=L on Dom(L)∩Ker(P)). The operator KP is the inverse operator of LP, defined by the following relation:
KP(x)(t)=∫t0x(τ)dτ−1ω∫ω0∫η0x(m)dmdη. | (B.1) |
To prove that KP=L−1P, we apply the following identity:
∫0ddsx(s)ds−1ω∫ω0∫0ddmx(m)dmdt=x(t), |
which is satisfied only on Dom(L)∩Ker(P).
(d) Considering the definition of the operator Q, we note that QN(x)=1ω∫ω0N(τ)dτ. Then, for x∈¯Ω we get that ‖QN(x)‖≤1ω∫ω0‖N‖dτ=‖N‖, which implies that QN(¯Ω) is bounded on ¯Ω. From the definitions of the operators KP,N and Q, we have the following:
(KP(I−Q)N))(x)(t)=∫t0N(τ)dτ+(12−tω)∫ω0N(τ)dτ−1ω∫ω0∫η0N(m)dmdη. |
Consequently, we deduce the estimate ‖KP(I−Q)N‖≤3ω‖N‖, thus indicating that (KP(I−Q)N)(¯Ω) is bounded on ¯Ω, as N is bounded on ¯Ω. Additionally, we clearly deduce that
|(KP(I−Q)N))(x)(t)−(KP(I−Q)N))(x)(s)|≤2‖N‖|t−s|,∀t,s∈[t0,∞], |
or equivalently, KP(I−Q)N is an equicontinuous operator. By applying Arzela-Ascoli's theorem, it follows that KP(I−Q)N is a compact operator on ¯Ω. Thereby, we conclude that N is L-compact on ¯Ω.
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Ps | Number of susceptible grapevines | (α)−1 | Average incubation time on grapevine |
Pe | Number of exposed grapevines | (γ)−1 | Average recovery time of infected grapevines |
Pi | Number of infected grapevines | μ | Mortality rate of vectors |
Vs | Number of susceptible vectors | (θ)−1 | Average incubation time in vector |
Ve | Number of Exposed Vectors | (κ)−1 | Average time of vector infection |
Vi | Number of infected vectors | (ν)−1 | Transmission rate of vectors |
Λ | Average insect vector birth rate | P | Total number of grapevines |
β | Infection rate of grapevines by vectors | V | Total number of vectors |
Ps | Number of susceptible grapevines | (α)−1 | Average incubation time on grapevine |
Pe | Number of exposed grapevines | (γ)−1 | Average recovery time of infected grapevines |
Pi | Number of infected grapevines | μ | Mortality rate of vectors |
Vs | Number of susceptible vectors | (θ)−1 | Average incubation time in vector |
Ve | Number of Exposed Vectors | (κ)−1 | Average time of vector infection |
Vi | Number of infected vectors | (ν)−1 | Transmission rate of vectors |
Λ | Average insect vector birth rate | P | Total number of grapevines |
β | Infection rate of grapevines by vectors | V | Total number of vectors |