RESUMEN

Parasite-induced modification of host behavior increasing transmission to a next host is a common phenomenon. However, field-based studies are rare, and the role of environmental factors in eliciting host behavioral modification is often not considered. We examined the effects of temperature, relative humidity (RH), time of day, date, and an irradiation proxy on behavioral modification of the ant Formica polyctena (Förster, 1850) by the brain-encysting lancet liver fluke Dicrocoelium dendriticum (Rudolphi, 1819). This fluke induces ants to climb and bite to vegetation by the mandibles in a state of temporary tetany. A total of 1264 individual ants expressing the modified behavior were observed over 13 non-consecutive days during one year in the Bidstrup Forests, Denmark. A sub-set of those ants (N = 172) was individually marked to track the attachment and release of infected ants in relation to variation in temperature. Infected ants primarily attached to vegetation early and late in the day, corresponding to low temperature and high RH, presumably coinciding with the grazing activity of potential herbivorous definitive hosts. Temperature was the single most important determinant for the induced phenotypic change. On warm days, infected ants altered between the manipulated and non-manipulated state multiple times, while on cool days, many infected ants remained attached to the vegetation all day. Our results suggest that the temperature sensitivity of the infected ants serves the dual purpose of exposing infected ants to the next host at an opportune time, while protecting them from exposure to high temperatures, which might increase host (and parasite) mortality.

RESUMEN

Recolonization of predators to their former ranges is becoming increasingly prevalent. Such recolonization places predators among their prey once again; the latter having lived without predation (from such predators) for a considerable time. This renewed coexistence creates opportunities to explore predation ecology at both fundamental and applied levels. We used a paired experimental design to investigate white-tailed deer risk allocation in the Upper and Lower Peninsulas (UP and LP) in Michigan, USA. Wolves are functionally absent in the LP, while deer in the UP coexist with a re-established wolf population. We treated 15 sites each in UP and LP with wolf olfactory cues and observed deer vigilance, activity, and visitation rates at the interface of habitat covariates using remote cameras. Such a paired design across wolf versus no-wolf areas allowed us to examine indirect predation effects while accounting for confounding parameters such as the presence of other predators and human activity. While wolf urine had no effect across most metrics in both UP and LP, we observed differences in deer activity in areas with versus without wolves. Sites treated with wolf urine in the UP showed a reduction in crepuscular deer activity, compared to control/novel-scent treated sites. Furthermore, we observed a strong positive effect of vegetation cover on deer vigilance in these sites. This indicates that simulated predator cues likely affect deer vigilance more acutely in denser habitats, which presumably facilitates predation success. Such responses were however absent among deer in the LP that are presumably naïve toward wolf predation. Where human and non-human predators hunt shared prey, such as in Michigan, predators may constrain human hunting success by increasing deer vigilance. Hunters may avoid such exploitative competition by choosing hunting/bait sites located in open areas. Our results pertaining to fundamental predation ecology have strong applied implications that can promote human-predator coexistence.

RESUMEN

Parasite species that use two or more host species during their life cycle depend on successful transmission between these species. These successive host species may have different habitat requirements. For example, one host species may be aquatic while the other is terrestrial. To overcome this complicating factor in transmission, a wide diversity of parasite species have adaptations that alter the habitat preference in one host species to facilitate transmission to the next host species.Two common trematode parasites in New Zealand, Atriophallophorus winterbourni and Notocotylus spp., both have a life cycle with two host species. The aquatic snail Potamopyrgus antipodarum is the intermediate host, from which the parasites require transmission to dabbling ducks or other waterfowl. Of these parasites, A. winterbourni is most frequently found in snails from the shallow-water margin. This may indicate parasite-induced movement of infected snails into the foraging habitat of dabbling ducks.To test whether the parasites manipulate the snails to move into shallow water, we stretched tubular mesh cages across depth-specific ecological habitat zones in a lake. Both infected and healthy snails were released into the cages. After 11 days, significantly higher infection frequencies of A. winterbourni were retrieved from the shallowest end of the cages, while Notocotylus spp. frequencies did not vary with depth.The hypothesis that A. winterbourni induces its snail host to move into the shallow-water habitat cannot be rejected based on the experimental results. Although further research is needed to address alternative explanations, the depth preference of infected snails may be due to a parasite adaptation that facilitates trophic transmission of parasites to dabbling ducks.

RESUMEN

The vegetable leafminer (Liriomyza sativae [Burgess]) is a highly polyphagous pest that threatens vegetables and horticultural plants. Although sexual communication is a key component of the animal behavioral repertoire, the mechanism underlying sexual communication in L. sativae remains to be elucidated. Here, we used laser vibrometry to characterize the vibrational signals emitted by L. sativae during pair formation. By emitting trains of vibrational pulses (male calling) the male initiated communication on the host plant. The female then became immobile and responded to the male calling by emitting replies (female replies), which in turn triggered male replies consisting of a rapid series of chirps and trills. If the female replied, a continuous exchange of male and female replies ensued, representing a duet. In playback trials, a playback signal caused responses from the opposite sex. Moreover, scanning electron microscopy revealed vibration-producing stridulatory organs in both male and female individuals. The files in males were more developed than those in females, and older male specimens had more signs of abrasion. The results provide new insight into the mating biology of L. sativae.

Asunto(s)

RESUMEN

The invasion of Drosophila suzukii, spotted-wing drosophila, across Europe and the US has led to economic losses for berry and cherry growers, and increased insecticide applications to protect fruit from damage. Commercial production relies heavily on unsustainable use of conventional toxic insecticides. Non-toxic insecticide strategies are necessary to alleviate the disadvantages and non-target impacts of toxic conventional insecticides and improve Integrated Pest Management (IPM). A novel food-grade gum deployed on dispenser pads (GUM dispensers) was evaluated to mitigate D. suzukii crop damage in five commercial crops and nine locations. Trials were conducted at a rate of 124 dispensers per hectare in cherry, wine grape, blueberry, raspberry, and blackberry in California and Oregon, USA during 2019 and 2020. The majority of trials with the food-grade gum resulted in a reduction of D. suzukii egg laying in susceptible fruit. In some cases, such damage was reduced by up to 78%. Overall, results from our meta-analysis showed highly significant differences between GUM treatments and the untreated control. Modeling simulations suggest a synergistic reduction of D. suzukii damage when used in combination with Spinosad (Entrust SC) insecticide. These data illustrate commercial value of this tool as a sustainable alternative to manage D. suzukii populations within a systems approach.

RESUMEN

A diversity of aquatic organisms manage predation risk by avoiding waters activated with conspecific alarm cues, a chemical mixture released from injuries. The sea lamprey (Petromyzon marinus) is a nocturnal migratory species that relies on its alarm cue to navigate around areas of predation risk when moving through river channels. Identification of the cue's chemistry would allow managers to harness this innate behavioral response to guide migrating sea lamprey to traps (invasive population in the Laurentian Great Lakes) or to fish passage devices where dams block migrations in their native range. We pursued isolation of the sea lamprey alarm cue through behaviorally guided fractionation, fractionating the alarm cue into water-soluble and chloroform-soluble fractions, each of which elicited a substantial avoidance response. Recombining the two fractions restored full reactivity, suggesting the alarm cue mixture contains components that exhibit high solubility in water (e.g., nitrogenous compounds), chloroform (e.g., lipids), or perhaps materials that dissolve readily in either solvent. We further screened 13 individual compounds or pure isolates and 6 sub-fractions from the water-soluble fraction and found one of the pure isolates, isoleucine, evoked an avoidance response on its own, but not consistently when found in other mixtures. In a third experiment, we observed no behavioral response after recombining 32 compounds isolated and identified from the water-soluble fraction. These results confirm other suggestions that the process of elucidating alarm cue constituents is challenging. However, we suggest the pursuit is worthwhile given the strong evidence for the utility of alarm cues for use in the conservation and management of fishes and other aquatic organisms.

Asunto(s)

RESUMEN

Horizontal transmission of the endosymbiont, Wolbachia, may occur during superparasitism when parasitoid females deposit a second clutch of eggs on a host. Wolbachia may increase the superparasitism tendency of Trichogramma wasps by depriving their memory. To test this hypothesis, we investigated the effects of conditioning experience and memory inhibitors (actinomycin D [ACD] and anisomycin [ANI]) on memory capacity, and expressions of memory-related genes (CREB1 and PKA), and superparasitism frequency of Wolbachia-infected (TDW) and uninfected (TD) lines of Trichogramma dendrolimi after conditioning with lemon or peppermint odor. We detected the presence of Wolbachia in eggs, larvae, pre-pupae, pupae, and adults of Trichogramma by using fluorescence in situ hybridization. The results showed that TDW females had a more reduced memory capacity than TD females after conditioning. Compared with TD females, TDW females showed a higher proportion of superparasitism and a downregulation of CREB1 and PKA genes after conditioning. TD females fed ACD or ANI showed a higher tendency for superparasitism and a downregulation of CREB1 and PKA, along with memory loss after conditioning than TD females fed honey solution only. The presence of Wolbachia was detected in the anterior region of the larva, pre-pupa, and pupa, but was not found in the head of the adult. The results provide evidence of host behavioral manipulation of Wolbachia by depriving memory of host Trichogramma wasps based on Poulin' s criteria. These host behavioral changes led by Wolbachia may be caused by the virulence of Wolbachia on the nervous system of the host. IMPORTANCE The endosymbiotic bacteria, Wolbachia, live widely within cells of arthropods. Wolbachia are not only transmitted vertically from host mother to offspring, but are also transmitted horizontally among host individuals. Horizontal transmission is expected to occur during superparasitism when host parasitoid females deposit a clutch of eggs on a host previously parasitized by the same parasitoid species. Thus, a question is proposed regarding whether superparasitism behavior is a behavior modification induced by the symbiont to favor symbiont transmission. This study highlights behavioral mechanisms of Wolbachia-induced superparasitism in Trichogramma wasps and the manipulation of symbionts on host parasitoids.

Asunto(s)

RESUMEN

Infection with the protozoan Toxoplasma gondii causes loss of innate fear of cat odors in both male and female rats. This behavioral change is presumed to reflect a parasitic manipulation that increases transmission of the parasite from its intermediate to definitive host. The host behavioral change in male rats is dependent on gonadal steroids. In contrast, the loss of fear in female rats is not accompanied by greater gonadal steroids and cannot be rescued by gonadectomy. This disparity suggests that proximate mechanisms of the post infection host behavioral change in rats are sexually dimorphic. Here, we report that female rats infected with Toxoplasma gondii exhibit greater abundance of messenger RNA for oxytocin and oxytocin receptors in the paraventricular nucleus of the hypothalamus and posterodorsal medial amygdala, respectively. Brain oxytocin is critical for sex-typical social and sexual behaviors in female rodents. The change in oxytocin and its receptor could potentially alter activity in the social salience circuits, leading to a reduction in defensive behaviors and an increase in approach to ambivalent environmental cues. Our results argue that sexually dimorphic neural substrates underpin sexually monomorphic host behavioral change in this host-parasite association.

RESUMEN

The fungal genus Entomophthora consists of highly host-specific pathogens that cause deadly epizootics in their various insect hosts. The most well-known among these is the "zombie fly" fungus E. muscae, which, like other Entomophthora species, elicits a series of dramatic behaviors in infected hosts to promote optimal spore dispersal. Despite having been first described more than 160 years ago, there are still many open questions about Entomophthora biology, including the molecular underpinnings of host behavior manipulation and host specificity. This review provides a comprehensive overview of our current understanding of the biology of Entomophthora fungi and enumerates the most pressing outstanding questions that should be addressed in the field. We briefly review the discovery of Entomophthora and provide a summary of the 21 recognized Entomophthora species, including their type hosts, methods of transmission (ejection of spores after or before host death), and for which molecular data are available. Further, we argue that this genus is globally distributed, based on a compilation of Entomophthora records in the literature and in online naturalist databases, and likely to contain additional species. Evidence for strain-level specificity of hosts is summarized and directly compared to phylogenies of Entomophthora and the class Insecta. A detailed description of Entomophthora's life-cycle and observed manipulated behaviors is provided and used to summarize a consensus for ideal growth conditions. We discuss evidence for Entomophthora's adaptation to growth exclusively inside insects, such as producing wall-less hyphal bodies and a unique set of subtilisin-like proteases to penetrate the insect cuticle. However, we are only starting to understand the functions of unusual molecular and genomic characteristics, such as having large > 1 Gb genomes full of repetitive elements and potential functional diploidy. We argue that the high host-specificity and obligate life-style of most Entomophthora species provides ample scope for having been shaped by close coevolution with insects despite the current general lack of such evidence. Finally, we propose six major directions for future Entomophthora research and in doing so hope to provide a foundation for future studies of these fungi and their interaction with insects.

RESUMEN

[This corrects the article DOI: 10.3389/fpsyt.2020.00630.].

RESUMEN

Many organisms are able to elicit behavioral change in other organisms. Examples include different microbes (e.g., viruses and fungi), parasites (e.g., hairworms and trematodes), and parasitoid wasps. In most cases, the mechanisms underlying host behavioral change remain relatively unclear. There is a growing body of literature linking alterations in immune signaling with neuron health, communication, and function; however, there is a paucity of data detailing the effects of altered neuroimmune signaling on insect neuron function and how glial cells may contribute toward neuron dysregulation. It is important to consider the potential impacts of altered neuroimmune communication on host behavior and reflect on its potential role as an important tool in the "neuro-engineer" toolkit. In this review, we examine what is known about the relationships between the insect immune and nervous systems. We highlight organisms that are able to influence insect behavior and discuss possible mechanisms of behavioral manipulation, including potentially dysregulated neuroimmune communication. We close by identifying opportunities for integrating research in insect innate immunity, glial cell physiology, and neurobiology in the investigation of behavioral manipulation.

Asunto(s)

RESUMEN

Semiochemical use is a promising way to reduce damage from pests by improving natural control in agro-ecosystems. The aphid alarm pheromone (E)-ß-farnesene (EßF) and herbivore-induced methyl salicylate (MeSA) are two volatile cues to induce changes in aphid behavior with functional significance. Because of limitations related to the volatility and oxidization of EßF and MeSA under natural conditions, slow-release and antioxidant techniques should be developed and optimized before application. Here, a slow-release alginate bead of EßF mixed with MeSA was first designed and manufactured. We hypothesized that a mixture of these two semiochemicals could be effective in controlling Sitobion miscanthi in wheat crops. Both MeSA and EßF in alginate beads were released stably and continuously for at least 15 days in the laboratory, whereas EßF in paraffin oil and pure MeSA were released for only 2 and 7 days, respectively. In 2018 field experiments, EßF and MeSA alone or in association significantly decreased the abundance of alate and apterous aphids. An increased abundance of mummified aphids enhanced by higher parasitism rates was observed when using EßF and MeSA in association, with a significant reduction of apterous abundance, more so than EßF or MeSA alone. In 2019, plots treated with a mixture of EßF and MeSA showed significantly decreased abundance of alate and apterous aphids with higher parasitism rates compared with the control. The new slow-release alginate bead containing a mixture of EßF with MeSA could be the most efficient formulation to control S. miscanthi population by attracting parasitoids in the wheat agro-ecosystem. © 2021 Society of Chemical Industry. © 2021 Society of Chemical Industry.

Asunto(s)

RESUMEN

Nonhuman primates (NHPs) have widely and crucially been utilized as model animals for understanding various higher brain functions and neurological disorders since their behavioral actions mimic both normal and disease states in humans. To know about how such behaviors emerge from the functions and dysfunctions of complex neural networks, it is essential to define the role of a particular pathway or neuron-type constituting these networks. Optogenetics is a potential technique that enables analyses of network functions. However, because of the large size of the NHP brain and the difficulty in creating genetically modified animal models, this technique is currently still hard to apply effectively and efficiently to NHP neuroscience. In this article, we focus on the issues that should be overcome for the development of NHP optogenetics, with special reference to the gene introduction strategy. We review the recent breakthroughs that have been made in NHP optogenetics to address these issues and discuss future prospects regarding more effective and efficient approaches to successful optogenetic manipulation in NHPs.

Asunto(s)

RESUMEN

Toxoplasma gondii is a protozoan parasite with a complex life cycle and a cosmopolitan host range. The asexual part of its life cycle can be perpetually sustained in a variety of intermediate hosts through a combination of carnivory and vertical transmission. However, T. gondii produces gametes only in felids after the predation of infected intermediate hosts. The parasite changes the behavior of its intermediate hosts by reducing their innate fear to cat odors and thereby plausibly increasing the probability that the definitive host will devour the infected host. Here, we provide a short description of such parasitic behavioral manipulation in laboratory rodents infected with T. gondii, along with a bird's eye view of underpinning biological changes in the host. We also summarize critical gaps and opportunities for future research in this exciting research area with broad implications in the transdisciplinary study of host-parasite relationships.

Asunto(s)

RESUMEN

Rats infected with the protozoan Toxoplasma gondii exhibit a reduced aversion to cat odor. This behavioral change is thought to increase trophic transmission of the parasite. Infected male rats also show a greater testicular synthesis of testosterone and epigenetic change in arginine vasopressin within the medial amygdala. Here, we show that exogenous supply of testosterone within MeA of uninfected castrates recapitulates reduction in innate fear akin to behavioral change attributed to the parasite. We also show that castration post establishment of chronic infection precludes changes in fear and medial amygdala arginine vasopressin in the infected male rats. These observations support the role of gonadal hormones and pursuant neuroendocrine changes in mediating the loss of fear in the infected rats. This work also demonstrates that testosterone acting specifically within the medial amygdala sufficiently explains reduced defensive behaviors often observed during the appetitive component of reproductive behaviors.

RESUMEN

Songbirds, such as the zebra finch, are a popular animal model for studying the neural basis of vocal and complex skill learning. Adult male zebra finches produce courtship song toward females (referred to as 'directed song') and recording and analyzing sounds of directed song along with underlying neural activity is important for investigating behavioral and neural mechanisms of song production and learning. However, recording of directed song is easily contaminated by calls that are often as loud as directed songs and frequently produced by a female bird is presented in the same sound-recording chamber to elicit directed song. We developed a new surgical procedure to relatively easily and almost completely devocalize female zebra finches semi-permanently, without affecting other behaviors. This procedure enables researchers to record directed songs with almost no contamination by female calls. The procedure can also be used to devocalize male birds as well and, thus, has great potential for a variety of experimental purposes, such as long-term elimination of auditory feedback during singing in male birds.

RESUMEN

Neurotoxoplasmosis, also known as cerebral toxoplasmosis, is an opportunistic chronic infection caused by the persistence of parasite Toxoplasma gondii cysts in the brain. In wild animals, chronic infection is associated with behavioral manipulation evident by an altered risk perception towards predators. In humans, reactivation of cysts and conversion of quiescent parasites into highly invasive tachyzoites is a significant cause of mortality in immunocompromised patients. However, the current standard therapy for toxoplasmosis is not well tolerated and is ineffective against the parasite cysts. In recent years, the concept of dietary supplementation with natural products derived from plants has gained popularity as a natural remedy for brain disorders. Notably, urolithin-A, a metabolite produced in the gut following consumption of ellagitannins-enriched food such as pomegranate, is reported to be blood-brain barrier permeable and exhibits neuroprotective effects in-vivo. In this study, we investigated the potential of pomegranate extract and urolithin-A as anti-neurotoxoplasmosis agents in-vitro and in-vivo. Treatment with pomegranate extract and urolithin-A reduced the parasite tachyzoite load and interfered with cyst development in differentiated human neural culture. Administration of urolithin-A also resulted in the formation of smaller brain cysts in chronically infected mice. Interestingly, this phenomenon was mirrored by an enhanced risk perception of the UA-treated infected mice towards predatory cues. Together, our findings demonstrate the potential of dietary supplementation with urolithin-A-enriched food as a novel natural remedy for the treatment of acute and chronic neurotoxoplasmosis.

RESUMEN

Some parasites have evolved the ability to adaptively manipulate host behavior. One notable example is the fungus Ophiocordyceps unilateralis sensu lato, which has evolved the ability to alter the behavior of ants in ways that enable fungal transmission and lifecycle completion. Because host mandibles are affected by the fungi, we focused on understanding changes in the metabolites of muscles during behavioral modification. We used High-Performance Liquid Chromatography-Mass/Mass (HPLC-MS/MS) to detect the metabolite difference between controls and O. unilateralis-infected ants. There was a significant difference between the global metabolome of O. unilateralis-infected ants and healthy ants, while there was no significant difference between the Beauveria bassiana treatment ants group compared to the healthy ants. A total of 31 and 16 of metabolites were putatively identified from comparisons of healthy ants with O. unilateralis-infected ants and comparisons of B. bassiana with O. unilateralis-infected samples, respectively. This result indicates that the concentrations of sugars, purines, ergothioneine, and hypoxanthine were significantly increased in O. unilateralis-infected ants in comparison to healthy ants and B. bassiana-infected ants. This study provides a comprehensive metabolic approach for understanding the interactions, at the level of host muscles, between healthy ants and fungal parasites.

Asunto(s)

RESUMEN

There are numerous examples of parasites that manipulate the behavior of the hosts that they infect. One such host-pathogen relationship occurs between the 'zombie-ant fungus' Ophiocordyceps unilateralis sensu lato and its carpenter ant host. Infected ants climb to elevated locations and bite onto vegetation where they remain permanently affixed well after death. The mandibular muscles, but not the brain, of infected ants are extensively colonized by the fungus. We sought to investigate the mechanisms by which O. unilateralis s.l. may be able to influence mandibular muscle contraction despite widespread muscle damage. We found that infected muscles show evidence of hypercontraction. Despite the extensive colonization, both motor neurons and neuromuscular junctions appear to be maintained. Infection results in sarcolemmal damage, but this is not specific to the death grip. We found evidence of precise penetration of muscles by fungal structures and the presence of extracellular vesicle-like particles, both of which may contribute to mandibular hypercontraction.

Asunto(s)

RESUMEN

In relation to behavioral changes in rodents infected with Toxoplasma gondii (T. gondii), it is believed that the genotype of the infecting strain can have some influence. In this sense, the present work has sought to evaluate the effect of chronic infection by genetically distinct cystogenic strains of T. gondii on the behavior of mice. For this, experimental models of infection with ME-49 (type II) and VEG (type III) strains were developed in isogenic BALB/c mice. ELISA test was performed to evaluate the humoral immune response and real-time PCR test to quantify parasites in the CNS. Behavioral tests such as passive avoidance, open-field and Y-maze tests were also used for, respectively, evaluation of learning and memory, locomotor activity and aversion to feline odor. The results showed that mice infected with VEG strain had higher total IgG level of anti-toxoplasma, higher tissue burden of T. gondii in the CNS, reduction in the long-term memory, lower activity (mobility) and lower aversion to cat urine and l-felinine than mice infected with ME-49 strain. The results suggest that different T. gondii genotypes have a differential impact on behavioral changes in infected mice.

Asunto(s)