Animal Behavior in Transmission of Vector-Borne Diseases

2.1 The blood-feeding imperative

Only female mosquitoes and sandflies blood-feed, and they do so as a prerequisite for egg development. This single biological fact places hematophagy at the center of VBD epidemiology. Blood-feeding behavior is not, however, a simple switch. As Tung and Fonseca [4] have comprehensively documented, blood-feeding in mosquitoes is a highly dynamic process shaped by the interaction of internal physiological states, nutritional status, gonotrophic cycle phase, hormonal signals, and external environmental cues, including light, temperature, humidity, and the chemical landscape of potential hosts.

The classic model of mosquito host-seeking assumed a fixed biting rate determined primarily by the gonotrophic cycle duration. This assumption, embedded in Ross’s vectorial capacity formula and subsequent mathematical models [5], has been increasingly challenged. Tung and Fonseca [4] argue persuasively that the functional response of vector biting rate to host density and the ideal free distribution of mosquitoes among available hosts are more realistic frameworks for modeling transmission risk. This has direct practical implications: High host density does not simply dilute transmission risk; it changes the behavioral ecology of vector–host contact in complex, nonlinear ways.

2.2 Sensory architecture of host location

The host location sequence in both mosquitoes and sandflies involves a hierarchical integration of sensory cues across increasing proximity. At long range (tens of meters), CO₂ exhaled by vertebrate hosts activates flight and upwind orientation. At medium range (one to five meters), body heat and volatile organic compounds (VOCs) from the skin refine host identification. At close range, visual cues, including the silhouette, color, and movement of a host, guide landing behavior [6, 7].

In Anopheles coluzzii, the primary malaria vector in West Africa, this sensory architecture is developmentally regulated. Teneral (newly emerged) females do not seek hosts immediately; the host-seeking drive develops over 24–72 hours posteclosion, coinciding with concerted upregulation of odorant receptor genes in both the antennae and maxillary palps [8]. This ontogenetic program represents one of the clearest examples of a timed, innate behavioral sequence hardwired by evolution to ensure the female is physiologically ready before she risks the energetic and predation costs of host-seeking.

The proboscis itself contributes to host identification, functioning as a “thermoantenna” that detects the thermal signature of subcutaneous blood vessels at distances of a few centimeters, providing the final targeting step before probing [7, 9]. This multistep, multimodal process from CO₂-triggered activation through thermal targeting is predominantly instinctive yet exquisitely tuned by selection to the thermal and chemical profile of the preferred host species.

2.3 Temporal patterns and biting periodicity

Anopheles gambiae sensu stricto is predominantly endophagic (biting indoors) and nocturnal, with peak biting occurring between 22:00 and 02:00 hours [10]. This temporal niche precisely overlaps the period when rural African households are occupied with sleeping unprotected individuals. This niche is not incidental; it is a product of evolutionary arms-race dynamics in which An. gambiae progressively specialized on humans during the agricultural revolution, coinciding with the expansion of dense, sedentary human populations [8] (Table 1).

Aedes aegypti, by contrast, is a diurnal biter with peak activity during the first two to three hours after sunrise and again in the late afternoon [7, 11]. Its domestic and peridomestic ecology means that biting occurs precisely when humans are most active indoors and in gardens. Jemberie et al. [7], conducting field studies in northwest Ethiopia, documented peak biting rates of 4.5 bites per person per hour between 07:00 and 08:00, a rate sufficient to sustain high dengue transmission in densely populated urban environments.

Phlebotomine sandflies are crepuscular, with the strongest activity at dusk and in the first half of the night. Their small size, with a wing length of only 1.5–3.5 mm, means they are poor fliers, confined to the lowest few meters of the air column, making their activity highly dependent on wind speed, temperature, and microhabitat structure. This crepuscular activity window creates a critical overlap with outdoor human and animal activity, particularly during the period when dogs and livestock are outside before being sheltered for the night [12] (Table 1).

2.4 Pathogen-induced behavioral manipulation

Perhaps the most striking dimension of vector behavior in VBD transmission is the growing evidence that pathogens actively manipulate vector behavior to enhance their own transmission [8]. The paradigmatic example in mosquito biology is the enhancement of host-seeking behavior in Anopheles gambiae infected with transmissible (sporozoite stage) Plasmodium falciparum. Sporozoite-infected mosquitoes are significantly more attracted to human odor than uninfected individuals or those carrying nontransmissible oocyst forms [8, 13].

This manipulation is temporally calibrated: The behavioral enhancement is specific to the sporozoite stage, the stage at which the parasite is ready for transmission, and is absent during the oocyst stage, when transmission would be futile. The molecular mechanism involves modulation of chemosensory gene expression and possibly salivary composition [8]. The net effect is a biologically elegant system in which the parasite fine-tunes its vector’s behavior to maximize contact with new hosts at precisely the moment when transmission is possible [13].

Analogous phenomena have been described in the Leishmania–sandfly system. Leishmania infantum infection causes physiological changes in the reservoir dog host that increase the dog’s attractiveness to Phlebotomus perniciosus sandflies. This enhanced attractiveness is likely mediated by alterations in the dog’s cutaneous volatile profile, meaning infected dogs attract more sandfly bites than uninfected dogs, thereby amplifying parasite transmission [12]. This represents a striking example of the parasite manipulating not the vector but the reservoir host to optimize its transmission cycle.

3.1 Behavioral defenses against vectors

Vertebrate hosts are not passive targets. They have evolved a diverse repertoire of behavioral defenses against hematophagous arthropods, ranging from simple mechanical responses to complex, socially organized parasite management strategies. A comprehensive review of programmed grooming, a centrally regulated, periodic behavior in ungulates, specifically calibrated to remove ectoparasites before they can fully blood-feed, provides compelling evidence that this behavior reduces tick burdens by 30–50% and operates on an internal schedule rather than being solely triggered by peripheral irritation [14, 15] (Table 2).

Dogs, the primary reservoir of zoonotic visceral leishmaniasis (ZVL) in the Mediterranean Basin and the Americas, illustrate the complex interplay between defensive behavior and parasite manipulation. Healthy dogs scratch and flee in response to sandfly bites, interrupting feeding events. However, as noted above, Leishmania infantum-infected dogs emit altered olfactory signals that make them more attractive to sandflies, effectively counteracting defensive behavior at the population level [12]. The parasite thus exploits the host’s sensory landscape to ensure preferential vector contact with the most infectious individuals in the reservoir population.

3.2 Movement behavior and spatial spread of disease

Animal movement behavior is a major determinant of VBD geographic spread and emergence. The errant behavior of stray dogs, a dimension of canine behavior with profound epidemiological consequences, is a key driver of the geographic expansion of canine visceral leishmaniasis (CVL) in urban Brazil and other endemic countries [3]. Vilas-Boas et al. [3] note that the combination of stray dog movement, high canine parasite loads on the skin, and the presence of peridomestic sandfly breeding habitats creates a self-reinforcing urban transmission cycle. Importantly, the peridomestic habitat – yards with trees, shade, and organic matter – is attractive to both sandflies and dogs, creating a spatial nexus for transmission.

Migratory wildlife movements similarly drive the spread of mosquito-borne viruses across geographic barriers. The northward expansion of dengue and Zika risk into previously nonendemic regions of Europe and North America has been driven not only by climate warming but by the combination of Aedes albopictus range expansion enabled by its behavioral tolerance of cooler temperatures and global human mobility that seeds new endemic foci [7, 16].

3.3 Roosting and shelter-seeking behavior

Where animals rest and shelter has direct consequences for their vector exposure. The cave-dwelling behavior of rock hyraxes (Heterohyrax brucei and Procavia capensis) in the Ethiopian highlands creates dense, predictable aggregations of the primary reservoir host for Leishmania aethiopica in precisely the microhabitats where Phlebotomus pedifer achieves its highest densities [12, 17]. Feeding choice experiments demonstrated that P. pedifer strongly prefers hyraxes over humans when both are available in cave settings, making the hyrax–sandfly interface in cave microhabitats the primary transmission nexus for cutaneous leishmaniasis in this system [12].

The indoor roosting behavior of humans, paradoxically, both creates and mitigates transmission risk. Indoor sleeping exposes individuals to endophilic vectors such as Anopheles gambiae, wherein indoor residual spraying (IRS) and insecticide-treated bed nets (ITBNs) exploit this behavioral overlap to achieve vector control. However, for Aedes aegypti, which bites primarily during daylight hours, traditional indoor-based interventions are far less effective, requiring behavior-informed strategies such as targeted outdoor larval source management and diurnal personal protection [6, 16].

4.1 Malaria – the Anopheles–plasmodium system

Malaria remains the world’s most lethal VBD, causing an estimated 249 million cases and 608,000 deaths in 2022 alone [1]. The behavioral biology of its primary African vectors – Anopheles gambiae sensu stricto, An. coluzzii, An. arabiensis, and An. funestus – is among the most extensively studied in vector entomology [8], yet new discoveries continue to reshape our understanding.

The An. gambiae complex illustrates how ecological specialization and behavioral traits coevolve. An. gambiae s.s. and An. coluzzii are predominantly anthropophilic (human-preferring) and endophagic, while An. arabiensis is more zoophilic and exophagic (biting outdoors). This differential host preference has direct consequences for malaria transmission intensity and for the effectiveness of indoor vector control. Modeling studies have shown that the sporozoite prevalence in An. gambiae fed on human versus bovine blood differs significantly, with human blood yielding higher sporozoite rates, suggesting that the parasite has coevolved with the host preference of its principal vector to maximize its developmental success [8] (Figure 1).

The deployment of ITNs and IRS over the past two decades has exerted significant selective pressure on An. gambiae behavior. There is mounting evidence that An. gambiae populations in highly ITN-covered regions are shifting toward earlier and more exophagic biting, a behavioral adaptation that avoids the insecticide barrier [10]. This is one of the most consequential examples of behavioral plasticity in a disease vector, with profound implications for malaria control strategies. Whether this shift represents genuine learning or rapid evolutionary change driven by selection for naturally occurring behavioral variants is a critical open question.

4.2 Dengue, Zika, and the Aedes aegypti urban interface

Aedes aegypti is arguably the most epidemiologically dangerous mosquito species in the twenty-first century. Its evolutionary trajectory from a forest-dwelling, animal-biting generalist (Ae. aegypti formosus) to the highly domesticated, human-specialized Ae. aegypti [6] represents one of the most striking examples of behavioral evolution driven by ecological opportunity. The domestic form has evolved a strong preference for human hosts, human-made water containers for oviposition, and indoor resting, creating near-perfect niche alignment with dense urban human populations (Figure 2).

Recent years have seen a dramatic global surge in Aedes-borne arboviral diseases. By June 2024, over 9.3 million dengue cases had been reported in the Americas alone [6], and a 2025 global distribution analysis confirmed an expanding geographic risk for dengue, chikungunya, Zika, and yellow fever into previously nonendemic temperate zones [18]. This expansion is behavioral as much as climatic: Ae. aegypti’s willingness to exploit a vast diversity of peridomestic and indoor water containers, from discarded tires to flower vases and cisterns, gives it a virtually unlimited larval habitat supply in human settlements worldwide [6, 16].

Multiple blood-feeding in Ae. aegypti, the tendency to interrupt feeding and resume on a different host within a single gonotrophic cycle, dramatically amplifies its epidemiological impact. While a mosquito that feeds to repletion on one host transmits to or from a single individual, an interrupted feeder may contact two, three, or more hosts in a single gonotrophic cycle. This behavior, driven at least partly by defensive host behavior (swatting, movement) that interrupts feeding, creates a behavioral bridge that accelerates intracommunity viral dissemination [6, 19].

5.1 Leishmaniasis – An overview of the transmission system

Leishmaniasis is a complex of protozoan diseases caused by over 20 Leishmania species, transmitted by approximately 30 sandfly species of medical importance globally. The WHO estimates 700,000 to one million new cases annually, with visceral leishmaniasis (VL, caused primarily by L. donovani and L. infantum) being potentially fatal if untreated, and cutaneous forms (CL) causing significant morbidity and stigma. Table 3 summarizes the primary reservoir hosts and key behavioral drivers of transmission across the major Leishmania species of veterinary and medical importance.

5.2 The dog as the central zoonotic reservoir

The domestic dog occupies a unique and pivotal position in the epidemiology of ZVL. Infected dogs carry high parasite burdens in the skin, the tissue from which sandflies acquire the parasite during blood-feeding, and maintain infection for months to years, providing a sustained reservoir for vector infection [3, 20]. Critically, Vilas-Boas et al. [3] note that the domestic dog’s key epidemiological importance derives not only from its biology but from its behavior: Dogs spend time both indoors and outdoors, move through neighborhoods, and share space with humans, creating multiple interface opportunities between sandfly populations and the human household.

The role of stray dogs warrants particular emphasis. Their errant movement behavior crossing neighborhood boundaries, visiting multiple households, and frequenting peridomestic areas attractive to sandflies, makes them highly effective vehicles for geographic dispersal of CVL [3, 16]. A 2024 systematic review of canine leishmaniasis in the Americas documented CVL in dogs from Uruguay to Canada and the USA, highlighting how the combination of canine mobility and increasing sandfly range expansion creates an expanding zoonotic risk landscape [16] (Table 3).

Perhaps the most behaviorally sophisticated dimension of the dog–Leishmania interface is the parasite’s manipulation of the reservoir host’s attractiveness to vectors. Infected dogs emit altered cutaneous volatile profiles that make them significantly more attractive to Phlebotomus perniciosus, the primary European vector of L. infantum, than uninfected dogs [12]. This host manipulation strategy, analogous to Plasmodium’s modulation of Anopheles behavior, ensures that the most infectious individuals in the reservoir population receive the most vector attention, optimizing parasite transmission at the population level (Table 3).

5.3 Sandfly behavioral ecology

The transmission ecology of Leishmania is shaped by the distinctive behavioral biology of Phlebotomine sandflies. Unlike mosquitoes, which can disperse over hundreds of meters to kilometers, sandflies typically remain within a few tens of meters of their resting and breeding sites, making microhabitat structure critically important for transmission risk [21].

Sandfly host preference varies markedly among species. Phlebotomus argentipes, the primary vector of L. donovani on the Indian subcontinent, feeds preferentially on cattle in its natural setting, but intensive IRS programs targeting human dwellings have driven a documented behavioral shift toward feeding on dogs and outdoor hosts [8]. This insecticide-driven host preference shift has significant implications: As L. donovani, classically considered anthroponotic, increasingly infects dogs in IRS-covered areas, a new zoonotic reservoir is being inadvertently created. This is a striking example of human intervention unwittingly altering the behavioral landscape of disease transmission.

In the Ethiopian highlands, the transmission ecology of L. aethiopica centers on the behavioral interface between Phlebotomus pedifer and its primary reservoir, the rock hyrax. Feeding choice experiments by Pareyn and colleagues demonstrated a statistically significant preference of P. pedifer for hyraxes over humans when both are available in cave settings [12]. The predominantly cave-resting behavior of hyraxes, their colonial social structure, and the high P. pedifer densities in cave microhabitats create a highly concentrated, recurring transmission interface that sustains a stable sylvatic transmission cycle. Human CL acquisition occurs when people enter caves or when hyraxes venture into peridomestic rocky areas near settlements (Figure 3).

6.1 The instinct–plasticity continuum in vectors

The question of whether arthropod disease vectors operate on purely instinctual programs or exhibit genuine behavioral plasticity is central to the theme of this volume. The evidence points firmly toward a continuum rather than a binary distinction. The basic motor programs of host-seeking – positive anemotaxis toward host odor, upwind flight, thermal targeting – are undeniably innate and are expressed in naive, laboratory-reared mosquitoes with no prior host experience. They represent the product of millions of generations of natural selection for efficient host location.

Yet superimposed on this innate framework is a surprising degree of plasticity. Associative learning, the ability to form conditioned associations between sensory stimuli and outcomes, has been demonstrated in Aedes aegypti. Mosquitoes that experience defensive behavior from a host during blood-feeding attempts subsequently show reduced attraction to that host’s odor in olfactometer assays, suggesting that aversive experience can modify a normally hardwired host-seeking response [19]. Whether this constitutes “learning” in a cognitively meaningful sense, or simply represents synaptic plasticity in sensory pathways, remains an open and fascinating question.

The developmental regulation of host-seeking in Anopheles coluzzii provides a different lens on this question. The timed ontogenetic switch from nectar-seeking to host-seeking behavior in young females [8] is unambiguously innate; it is expressed identically in naive laboratory colonies and wild-caught individuals, and it is linked to precisely timed changes in odorant receptor expression that are presumably genetically encoded. Yet the specific sensory cues that activate host-seeking, and the threshold of response, are modified by gonotrophic state, infection status, and prior experience. The architecture is instinctual; the tuning is plastic.

6.2 Host behavioral flexibility and disease outcomes

On the host side, the programmed grooming model of Hart and Hart [14] provides compelling evidence for a centrally regulated, innate parasite management system in ungulates that is calibrated by evolutionary history to the parasite pressure experienced by each species. This is grooming as a fixed action pattern triggered by an internal clock rather than solely by peripheral irritation, which represents the host’s innate immune strategy at the behavioral level.

Yet vertebrate hosts also show genuine flexibility in antivector behavior. Birds that nest in high-mosquito environments develop more vigorous and frequent defensive behaviors than conspecifics from low-exposure environments [22]. Dogs that have experienced sandfly exposure may develop altered skin immune responses that reduce sandfly feeding success, an immunological analog of learned resistance [11]. These examples suggest that the boundary between instinct and adaptive flexibility is as permeable in the host as in the vector.

The One Health insight is that these behavioral systems, innate and flexible, in vectors and hosts alike, do not operate in isolation. They coevolve, with pathogens as the invisible selective force shaping both. Understanding this coevolutionary dynamic is essential for designing interventions that are robust to behavioral adaptation by vectors and robust to the disruption of host defensive behavior by pathogens.

7.1 Urbanization

Urbanization is the dominant ecological process of reshaping VBD transmission globally. The interaction between Aedes aegypti’s domestic behavior and urban environments is the most extensively documented example [6, 16]. Unplanned urban growth in tropical and subtropical regions creates vast expanses of informal settlements that provide abundant larval breeding sites, dense human populations, and reduced access to vector control services, a near-perfect environment for peridomestic dengue transmission. Facchinelli et al. [18] have argued that essentially all the biological-behavioral traits of Ae. Aegypti – its anthropophilic nature, its preference for small water containers, and its tendency to enter houses – can be understood as evolutionary adaptations to urban human environments, representing one of the most successful behavioral specializations in the insect world.

Urbanization similarly drives the emergence of CVL in new urban foci. The migration of rural populations (and their dogs) into cities, combined with the periurban habitats created by rapid, unplanned expansion, has generated a series of urban ZVL emergence events across Brazil and other South American countries. In each case, the causal mechanism involves a behavioral nexus: Dogs move into sandfly habitat zones, sandflies are present at the urban–rural interface, and the human infrastructure to detect and manage CVL is inadequate [3, 16].

7.2 Climate change and deforestation

Climate change expands the geographic zones where temperature and humidity support sandfly and mosquito populations, effectively extending the temporal and spatial range of transmission [18, 23]. But climate change also operates through behavior: Warming temperatures shift the diel activity windows of vectors, potentially creating novel mismatches between vector biting times and existing control measure schedules. A warmer climate may also compress the extrinsic incubation period of arboviruses within Ae. aegypti, increasing the proportion of the vector population that is infectious at any given time – a direct enhancement of the transmission consequences of the mosquito’s existing biting behavior [4].

Deforestation is a major driver of leishmaniasis emergence in the Americas. As forest is cleared, the sylvatic transmission cycle involving forest rodents, marsupials, and canopy-dwelling sloths as reservoir hosts of L. braziliensis and related species is disrupted, forcing vectors into peridomestic settings and placing human settlers and their animals directly in the transmission pathway. This environmental transformation essentially rewrites the behavioral geography of transmission: Vectors that previously fed on wildlife now encounter dogs and humans, creating conditions for zoonotic spillover [16, 21].