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Determining how ant colonies optimize foraging while mitigating pathogen and predator risks provides insight into how the ants have achieved ecological success. Ants must respond to changing resource conditions, but exploration comes at a cost of higher potential exposure to threats. Fungal infected cadavers surround the main foraging trails of the carpenter ant Camponotus rufipes, offering a system to study how foragers behave given the persistent occurrence of disease threats. Studies on social insect foraging behavior typically require many hours of human labor due to the high density of individuals. To overcome this, we developed deep learning based computer vision algorithms to track foraging ants, frame-by-frame, from video footage shot under the natural conditions of a tropical forest floor at night. We found that most foragers walk in straight lines overlapping the same areas as other ants, but there is a subset of foragers with greater exploration. Consistency in walking behavior may protect most ants from infection, while foragers that explore unique portions of the trail may be more likely to encounter fungal spores implying a trade-off between resource discovery and risk avoidance.

The fall armyworm, Spodoptera frugiperda (FAW), first invaded Africa in 2016 and has since become established in many areas across the continent where it poses a serious threat to food and nutrition security. We re-parameterized the existing CLIMEX model to assess the FAW global invasion threat, emphasizing the risk of transient and permanent population establishment in Africa under current and predicted future climates, considering irrigation patterns. FAW can establish itself in almost all countries in eastern and central Africa and a large part of western Africa under the current climate. Climatic barriers, such as heat and dry stresses, may limit the spread of FAW to North and South Africa. Future predictions suggest that FAW invasive range will retract from both northern and southern regions towards the equator. However, a large area in eastern and central Africa is predicted to have an optimal climate for FAW persistence. These areas will serve as FAW ‘hotspots’ from where it may migrate to the north and south during winter seasons and then pose an economic threat. Our projections can be used to identify countries at risk for permanent and transient FAW-population establishment and inform timely integrated pest management interventions under present and future climate in Africa.

Ophiocordyceps species infecting ants – the so-called zombie-ant fungi – comprise one of the most intriguing and fascinating relationships between microbes and animals. They are widespread within tropical forests worldwide, with relatively few reports from temperate ecosystems. These pathogens possess the ability to manipulate host behaviour in order to increase their own fitness. Depending on the fungal species involved the infected ants are manipulated either to leave the nest to ascend understorey shrubs, to die biting onto vegetation, or descend from the canopy to die at the base of trees. Experimental evidence has demonstrated that the behavioural change aids spore dispersal and thus increases the chances of infection, because of the existing behavioural immunity expressed inside ant colonies that limits fungal development and transmission. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe 15 new species of Ophiocordyceps with hirsutella-like asexual morphs that exclusively infect ants. These form a monophyletic group that we identified in this study as myrmecophilous hirsutelloid species. We also propose new combinations for species previously described as varieties and provide for the first time important morphological and ecological information. The species proposed herein were collected in Brazil, Colombia, USA, Australia and Japan. All species could readily be separated using classic taxonomic criteria, in particular ascospore and asexual morphology. Key words: Behaviour manipulation, Camponotini, Entomopathogenic fungi, Host association, Hypocreales, Insect pathogen, Multigene phylogeny, Ophiocordyceps, Ophiocordyceps unilateralis, Zombie-ant fungi, Taxonomic novelties: new combinations: Ophiocordyceps dolichoderi (H.C. Evans & Samson) Araújo, H.C. Evans & D.P. Hughes, O. monacidis (H.C. Evans & Samson) Araújo, H.C. Evans & D.P. Hughes, new species: O. albacongiuae Araújo, H.C. Evans & D.P. Hughes, O. blakebarnesii Araújo, H.C. Evans & D.P. Hughes, O. camponoti-chartificis Araújo, H.C. Evans & D.P. Hughes, O. camponoti-femorati Araújo, H.C. Evans & D.P. Hughes, O. camponoti-floridani Araújo, H.C. Evans & D.P. Hughes, O. camponoti-hippocrepidis Araújo, H.C. Evans & D.P. Hughes, O. camponoti-nidulantis Araújo, H.C. Evans & D.P. Hughes, O. camponoti-renggeri Araújo, H.C. Evans & D.P. Hughes, O. camponoti-sexguttati Araújo, H.C. Evans & D.P. Hughes, O. daceti Araújo, H.C. Evans & D.P. Hughes, O. kimflemingiae Araújo, H.C. Evans & D.P. Hughes, O. naomipierceae Araújo, H.C. Evans & D.P. Hughes, O. oecophyllae Araújo, S. Abell, T. Marney, R. Shivas H.C. Evans & D.P. Hughes, O. ootakii Araújo, H.C. Evans & D.P. Hughes., O. satoi Araújo, H.C. Evans & D.P. Hughes

Animal movement often exhibits changing behavior because animals often alternate between exploring, resting, feeding, or other potential states. Changes in these behavioral states are often driven by environmental conditions or the behavior of nearby individuals. We propose a model for dependence among individuals’ behavioral states. We couple this state switching with complex discrete-time animal movement models to analyze a large variety of animal movement types. To demonstrate this method of capturing dependence, we study the movements of ants in a nest. The behavioral interaction structure is combined with a spatially varying stochastic differential equation model to allow for spatially and temporally heterogeneous collective movement of all ants within the nest. Our results reveal behavioral tendencies that are related to nearby individuals, particularly the queen, and to different locations in the nest.

Interactions lie at the heart of social organization, particularly in ant societies. Interaction rates are presumed to increase with density, but there is little empirical evidence for this. We manipulated density within carpenter ant colonies of the species Camponotus pennsylvanicus by quadrupling nest space and by manually tracking 6.9 million ant locations and over 3200 interactions to study the relationship between density, spatial organization and interaction rates. Colonies divided into distinct spatial regions on the basis of their underlying spatial organization and changed their movement patterns accordingly. Despite a reduction in both overall and local density, we did not find the expected concomitant reduction in interaction rates across all colonies. Instead, we found divergent effects across colonies. Our results highlight the remarkable organizational resilience of ant colonies to changes in density, which allows them to sustain two key basic colony life functions, that is food and information exchange, during environmental change.

Determining how ant colonies optimize foraging while mitigating disease risk provides insight into how the ants have achieved ecological success. Fungal infected cadavers surround the main foraging trails of the carpenter antCamponotus rufipes, offering a system to study how foragers behave given the persistent occurrence of disease threats. Studies on social insect foraging behavior typically require many hours of human labor due to the high density of individuals. To overcome this, we developed deep learning based computer vision algorithms to track foraging ants, frame-by-frame, from video footage. We found foragers can be divided into behavioral categories based on how straight they walk across the trail. Eighty percent of ants walk directly across the trail, while 20% wander or circle when crossing the trail. Departure from the main trail encourages exploration of new areas and could enhance discovery of new food resources. Conversely, results from our agent-based model simulations suggest deviation from a straight path exposes foragers to more infectious fungal spores. Consistency in walking behavior may protect most ants from infection, while the foragers with increased exposure due to their mode of walking could be a sufficient number of new hosts to sustain disease in this environment.

1.AbstractAnts are among the most ecologically successful organisms on Earth, with a global distribution and diverse nesting and foraging ecologies. Ants are also social organisms, living in crowded, dense colonies that can range up to millions of individuals. Understanding the ecological success of the ants requires understanding how they have mitigated one of the major costs of social living-infection by parasitic organisms. Additionally, the ecological diversity of ants suggests that they may themselves harbor a diverse, and largely unknown, assemblage of parasites. As a first step, we need to know the taxonomic and functional diversity of the parasitic organisms infecting ants. To that end, we provide a comprehensive review of the parasitic organisms infecting ants by collecting all extant records. We synthesize major patterns in parasite ecology by categorizing how parasites encounter their ant hosts, whether they require host death as a developmental necessity, and how they transmit to future hosts.We report 1,415 records of parasitic organisms infecting ants, the majority of which come from order Diptera (34.8%), phylum Fungi (25.6%), and order Hymenoptera (25.1%). Most parasitic organisms infecting ants are parasitoids (89.6%), requiring the death of their host as developmental necessity and most initially encounter their hosts in the extranidal environment (68.6%). Importantly, though most parasitic organisms infecting ants only need a single host to complete their life cycle (89.2%), the vast majority need to leave the nest before transmission to the next ant host can occur (88.3%), precluding ant-to-ant transmission within the nest. With respect to the host, we only found records for 9 out of 17 extant ant sub-families, and for 82 out of the currently recognized 334 ant genera. Though there is likely bias in the records reported, both host and parasite ecological traits and evolutionary histories underlie the pattern of ant-parasite association reported here. This work provides a foundation for future work that will begin to untangle the ecological drivers of ant-parasite relationships and the evolutionary implications thereof.

Environmental conditions exert strong selection on animal behavior. We tested the hypothesis that the altered behavior of hosts due to parasitic manipulation is also subject to selection imposed by changes in environmental conditions over time. Our model system is ants manipulated by parasitic fungi to bite onto vegetation. We analyzed the correlation between forest type (tropical vs. temperate) and biting substrate (leaf vs. twigs), the time required for the fungi to reach reproductive maturity, and the phylogenetic relationship among specimens from tropical and temperate forests in different parts of the globe. We show that the fungal development in temperate forest is longer than the period of time leaves are present and the ants are manipulated to bite twigs. When biting twigs, 90% of the we examined dead ants had their legs wrapped around twigs, which appears to provide better attachment to the plant. Ancestral state character reconstruction suggests that the leaf biting is the ancestral trait and that twig biting is a convergent trait in temperate regions of the globe. These three lines of evidence suggest that changes in environmental conditions have shaped the manipulative behavior of the host by its parasite.

Synopsis Co-evolution of parasites and their hosts has led to certain parasites adaptively manipulating the behavior of their hosts. Although the number of examples from different taxa for this phenomenon is growing, the mechanisms underlying parasite-induced manipulation of hosts’ behavior are still poorly understood. The development of laboratory infections integrating various disciplines within the life sciences is an important step in that direction. Here, we advocate for such an integrative approach using the parasitic fungi of the genus Ophiocordyceps that induce an adaptive biting behavior in Camponotus ants as an example. We emphasize the use of behavioral assays under controlled laboratory conditions, the importance of temporal aspects of the behavior (possibly involving the circadian clock), and the need to approach colonizing parasites as organizations with a division of labor.

Ants, like any animal, are subject to parasitism. However, as they are also superorganisms living in common nests, their parasites experience environments wholly different from those of parasites affecting solitary organisms [1]. The nests of most ant species are relatively stable microhabitats prone to provide both readily available resources and some degree of protection against predators to many organisms. Consequently, ant-parasite (or ant-myrmecophile) associations gather a great deal of diversity ranging from the casual, opportunistic, unspecialized interaction—through temporary protection or sharing of some resources or even predation—, to obligate, specific mutualism that may involve coevolution of both the host and the parasite [2–5]. The first issue of this series examined a wide range of species: viruses, bacteria, fungi, nematodes, silverfishes, flies, butterflies, beetles, spiders, wasps, and ants themselves. However, it could not cover all possible ant parasites. More studies examining their complex interactions from every possible angle, attempting to bring a more global vision of the functioning of such an evolutionary important relationship , are a challenging and fascinating goal. In this second volume, we continued giving specific attention to both the mechanisms used by ant parasites to integrate into their host colony and the way parasite pressure could affect patterns of reproduction and life history in ant hosts. Moreover, considering the increasing pace of losses in biodiversity due to habitat destruction and climate change, we also wanted to reflect the effort towards accurate faunistic surveys of the diversity of the associations involving ants as hosts and the exact nature of these associations. This volume is divided into two main sections: (1) ant-parasite interactions and the mechanisms of integration into the host colony, in which both already known and new associations between ants and a diverse fauna including numerous beetle families, phorid and syrphid flies, diapriid, eucharitid and eurytomid wasps, myrmecophilid crickets, spiders, and bacteria are reviewed and/or discussed considering behavioral, taxonomical, phylogenetical, and even conceptual aspects; (2) social parasitism involving ant-ant interactions, in which different interspecific associations between ant species are reviewed, from the most basic forms illustrated by independent plesiobiotic associations to sophisticated, permanent ones found between slave-making ants or inquiline species and their single specialized hosts.

Ophiocordyceps unilateralis (Ascomycota: Hypocreales) is a specialized parasite that infects, manipulates and kills formicine ants, predominantly in tropical forest ecosystems. We have reported previously, based on a preliminary study in remnant Atlantic Forest in Minas Gerais (Brazil), that O. unilateralis represents a species complex. On each of the four species of infected carpenter ant (Camponotus) collected, the fungus – characterized macroscopically by a single stalk arising from the dorsal neck region on which the sexual structures (stromatal plates) are borne laterally – can readily be distinguished both microscopically and functionally. Here, we describe and discuss the biology, life cycle and infection strategies of O. unilateralis s.l. and hypothesize that there may be hundreds of species within the complex parasitizing formicine ants worldwide. We then address the diversity within related hypocrealean fungi, with particular reference to symbionts (mutualists through to parasites), and argue that the widely-quoted total of extant fungi (1.5 million species) may be grossly underestimated.

Parasites commonly manipulate host behaviour, and among the most dramatic examples are diverse fungi that cause insects to die attached to leaves. This death-grip behaviour functions to place insects in an ideal location for spore dispersal from a dead body following host death. Fossil leaves record many aspects of insect behaviour (feeding, galls, leaf mining) but to date there are no known examples of behavioural manipulation. Here, we document, to our knowledge, the first example of the stereotypical death grip from 48 Ma leaves of Messel, Germany, indicating the antiquity of this behaviour. As well as probably being the first example of behavioural manipulation in the fossil record, these data support a biogeographical parallelism between mid Eocene northern Europe and recent southeast Asia.

The leaf-cutting ants practise an advanced system of mycophagy where they grow a fungus as a food source. As a consequence of parasite threats to their crops, they have evolved a system of morphological, behavioural, and chemical defences, particularly against fungal pathogens (mycopathogens). 2. Specific fungal diseases of the leaf-cutting ants themselves have not been described, possibly because broad spectrum anti-fungal defences against mycopathogens have reduced their susceptibility to entomopathogens. 3. Using morphological and molecular tools, the present study documents three rare infection events of Acromyrmex and Atta leaf-cutting ants by Ophiocordyceps fungi, a genus of entomopathogens that is normally highly specific in its host choice. 4. As leaf-cutting ants have been intensively studied, the absence of prior records of Ophiocordyceps suggests that these infections may be a novel event and that switching from one host to another is possible. To test the likelihood of this hypothesis, host switching was experimentally induced, and successfully achieved, among five distinct genera of ants, one of which was in a different sub-family than the leaf-cutter ants. 5. Given the substantial differences among the five host ants, the ability of Ophiocordyceps to shift between such distant hosts is remarkable; the results are discussed in the context of ant ecological immunology and fungal invasion strategies.

The massive environmentally buffered nests of some social insects can contain millions of individuals and a wide variety of parasites, commensals and mutualists. We suggest that the ways in which these homeostatic fortress environments affect the evolution of social insect symbionts are relevant for epidemiology, evolutionary biology and macroecology. We contend that specialized parasites will tend to become less virulent and mutualists less cooperative, compared to those associated with solitary or small-colony hosts. These processes are expected to contribute to the very high symbiont diversity observed in these nests. We hypothesize that biodiversity gradients in these hotspots might be less affected by abiotic latitudinal clines than gradients in neighboring 'control' habitats. We suggest several research lines to test these ideas.

International audience; The hairworm (Nematomorpha) Paragordius tricuspidatus has the ability to alter the behaviour of its terrestrial insect host (the cricket Nemobius sylvestris), making it jump into the water to reach its reproductive habitat. Because water is a limited and critical resource in the ecosystem, we predicted that hairworms should adaptively manipulate host behaviour to maximize parasite reproductive success. Our results supported the hypothesis that the host manipulation strategy of hairworms consists of at least two distinct steps, first the induction of erratic behaviour and then suicidal behaviour per se. Hairworms secured mating by starting to manipulate their host before being fully mature. Once induced, the cricket's suicidal behaviour was maintained until the host found water but the fecundity of worms decreased over time. As expected, the fecundity of worms was better in crickets with suicidal rather than erratic behaviour.

Parasites can manipulate the behavior of their hosts in ways that increase either their direct fitness or transmission to new hosts. The Kingdom Fungi have evolved a diverse array of strategies to manipulate arthropod behavior resulting in some of the most complex and impressive examples of behavioral manipulation by parasites. Here we provide an overview of these different interactions and discuss them from an evolutionary perspective. We discuss parasite manipulation within the context of Niko Tinbergen's four questions (function, phylogeny, causation, and ontogeny) before detailing the proximate mechanisms by which fungi control arthropod behavior and the evolutionary pathways to such adaptations. We focus on some systems for which we have recently acquired new knowledge (such as the zombie ant fungus, Ophiocordyceps unilateralis s.l.), but a major goal is also to highlight how many interesting examples remain to be discovered and investigated. With this in mind, we also discuss likely examples of manipulated spiders that are largely unexplored ("zombie spiders"). Armed with advanced tools in evolutionary biology (from serial block face SEM to RNAseq) we can discover how the fungi, a group of microbes capable of coordinated activity, have evolved the ability to direct animal behavior. In short, we have the ability to understand how the organism without the brain controls the one with the brain. We hope such a goal, coupled with the knowledge that many diverse examples of control exist, will inspire other organismal biologists to study the complex adaptations that have arisen from "so simple a beginning."

It is assumed that social life can lead to the rapid spread of infectious diseases and outbreaks. In ants, disease outbreaks are rare and the expression of collective behaviors is invoked to explain the absence of epidemics in natural populations. Here, we address the ecological approach employed by many studies that have notably focused (89% of the studies) on two genera of generalist fungal parasites ( Beauveria and Metarhizium ). We ask whether these are the most representative models to study the evolutionary ecology of ant–fungal parasite interactions. To assess this, we critically examine the literature on ants and their interactions with fungal parasites from the past 114 years (1900–2014). We discuss how current evolutionary ecology approaches emerged from studies focused on the biological control of pest ants. We also analyzed the ecological relevance of the laboratory protocols used in evolutionary ecology studies employing generalist parasites, as well as the rare natural occurrence of these parasites on ants. After a detailed consideration of all the publications, we suggest that using generalist pathogens such as Beauveria and Metarhizium is not an optimal approach if the goal is to study the evolutionary ecology of disease in ants. We conclude by advocating for approaches that incorporate greater realism.

High-density living is often associated with high disease risk due to density-dependent epidemic spread. Despite being paragons of high-density living, the social insects have largely decoupled the association with density-dependent epidemics. It is hypothesized that this is accomplished through prophylactic and inducible defenses termed ‘collective immunity’. Here we characterise segregation of carpenter ants that would be most likely to encounter infectious agents (i.e. foragers) using integrated social, spatial and temporal analyses. Importantly, we do this in the absence of disease to establish baseline colony organization. Behavioural and social network analyses show that active foragers engage in more trophallaxis interactions than their nest worker and queen counterparts and occupy greater area within the nest. When the temporal ordering of social interactions is taken into account, active foragers and inactive foragers are not observed to interact with the queen in ways that could lead to the meaningful transfer of disease. Furthermore, theoretical resource spread analyses show that such temporal segregation does not appear to impact the colony-wide flow of food. This study provides an understanding of a complex society’s organization in the absence of disease that will serve as a null model for future studies in which disease is explicitly introduced.

In tropical forests, one of the most common relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. These fungi have the ability to penetrate the exoskeleton of the ant and to manipulate the behavior of the host, making it leave the nest and ascend understorey shrubs, to die biting onto the vegetation: hence, the term zombie-ant fungi to describe this behavioral changes on the host. It is posited that this behavioral change aids spore dispersal and thus increases the chances of infection. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe multiple new and host-specific species of the genus Ophiocordyceps on Camponotus and Polyrhachis ants from the central Amazonian region of Brazil, USA, Australia and Japan, which can readily be separated using classic taxonomic criteria, in particular ascospore morphology.

An important factor modulating parasite virulence is the level of extrinsic mortality experienced by hosts. Where it is high, parasites are expected to grow or reproduce quickly to complete their lifecycle before their host is killed, whereas virulence is expected to be less under low extrinsic mortality, where growth/reproduction can be slower. A prominent example of a low mortality environment for parasites are immature social insects. Here we examined the cost of parasitism, i.e. virulence, experienced by larval and pupal stages of Polistes wasps following infection by endoparasitic Strepsiptera (under starvation conditions). We found that there was no difference in virulence between infected and uninfected individuals for the seven days following infection; either measured as host mortality or mass loss. Likewise, there was no observed cost of parasitism during the first seven days of the pupal stage of the host. Growth of the endoparasitic stages appeared the same between starved laboratory individuals and field caught samples. Strepsipteran parasites apparently enter a lag phase until the later stages of host pupal development, which we speculate reduces the negative impact of parasitism during the hosts' critical developmental stages. Our results highlight the need for further inquiry into the influence of sociality upon the evolution of parasite virulence.

The incidence of strepsipteran parasites in temperate Polistes wasps is recorded following the collection and dissection of adults from nests, foraging sites and hibernacula. The mean proportion of infected P. dominulus adults (i.e. parasite prevalence) on nests was around 7%, while wasps which were captured when hunting for prey or collecting water were rarely parasitized. Of the four Polistes species that were recovered from overwintering aggregations (dominulus, gallicus, nimphus and associus) only P. gallicus was uninfected. In P. dominulus, the most numerous host sampled, up to 25% of overwintering females were infected. We discuss our findings in the light of an extensive collation of records of Polistes parasitized by the strepsipteran genus Xenos in old and recent literature.

Infection of the paper wasp, Polistes dominulus (Christ), by the strepsipteran parasite Xenos vesparum Rossi results in a dramatic behavioral change, which culminates in colony desertion and the formation of extranidal aggregations, in which up to 98% of occupants are parasitized females. Aggregations formed on prominent vegetation, traditional lek-sites of Polistes males, and on buildings, which were later adopted as hibernating sites by future queens. First discovered by W.D. Hamilton, these aberrant aggregations are an overlooked phenomenon of the behavioral ecology of this intensively studied wasp. For 3 months in the summer of 2000, during the peak of colony development, we sampled 91 extranidal aggregations from seven areas, numbering 1322 wasps. These wasps were parasitized by both sexes of X. vesparum, but males were more frequent from July until mid-August, during the mating season of the parasite. Aggregations were present for days at the same sites (in one case a leaf was occupied for 36 consecutive days) and were characterized by extreme inactivity. After artificial infection, parasitized ‘‘workers’’ deserted the nest 1 week after emergence from their cell and before the extrusion of the parasite through the host cuticle. Infected individuals did not work, were more inactive, and did not receive more aggression than did controls. We suggest that early nest desertion and subsequent aggregations by parasitized nominal workers and ‘‘future queens’’ is adaptive manipulation of host behavior by the parasite to promote the completion of its life cycle. Key words: aggregation, behavioral manipulation, nest desertion, Polistes, Strepsiptera. [Behav Ecol 15:1037–1043 (2004)]

Summary. Though the paper wasp genus, Polistes, is well studied, we know little of the incidence of parasitism in this group. Here we present details of 45 nest dissections for 4 species: P. dominulus (Christ), P. g allicus (L.), P. stabilinus Richards and P. carnifex (F.) to detail levels of parasitism of colony members by the obligate parasitic group of insects, the Strepsiptera. All 4 species showed evidence of parasitism among immature members. For 3 species, more than 50% of inspected nests were parasitized and the levels of parasitism among brood (larvae and pupae) was very high and did not differ significantly between parasitized nests. One species, P. stabilinus, suffered very low levels of parasitism, which may be related to its habitat choice. The number of parasites per host was positively related to the proportion of infected brood (parasite prevalence) and in some cases reached phenomenally high levels, which casts doubt on previously assumed mechanisms of infection for nest-making Hymenoptera, i.e. phoresy. We also document cases of egg parasitism and encapsulation in Polistes nests. Our data show that parasitism levels greatly varied among areas. Finally, the recent debate on the competitive advantage of P. dominulus in its introduced range, USA, has credited an absence of strepsipteran parasites of this species in facilitating its spread. For the first time, we document levels of parasitism for this species in its nature P range and this would appear to corroborate previous claims. We place our work in the context of other studies of parasitism of social insects and posit that the genus Polistes may have much to offer to this field.

The male of Caenocholax fenyesi Pierce (Strepsiptera) is widespread in SouthAmerica, but no host records are known as the specimens examined were free-living males that came into traps. In southern USA C.fenyesi was found to parasitize the red imported Þre ant, Solenopsiswagneri Santschi (Hymenoptera: Formicidae). We found a nest of the carpenter ant, Camponotus planatus Roger, in Veracruz, Mexico to be parasitized by C. fenyesi. This is the Þrst record of a host of C. fenyesi from the Neotropics. At the same location Pierce (1909) found the type species of C. fenyesi, but there were no host records. As our Þndings were from the same location, we speculate whether C. planatus is the endemic host of C. fenyesi. If so, did C. fenyesi arrive in southern USA parasitic on C. planatus, and move to an exotic host, S. wagneri in an alien enviroment? We also synonomize Myrmecolax ogloblini Luna de Carvalho and Caenocholax brasiliensis Oliveira & Kogan from Brazil with C. fenyesi, based on the unique structure of the aedeagus of the latter.

It has been remarked upon by Robert May (MAY 2001) that to write a paper with Bill Hamilton admitted one to a small circle, the honour of inclusion in which was not lost upon him. Equally, I think, a similar circle exits for people who can say they were students of Bill’s. For a brief time I was co-supervised by Bill (and principally by Jeyaraney Kathirithamby). As his student I have found that I hold some imaginary identification card that allows me to garner information from numerous sources about various aspects of Bill’s life. The esteem and reverence that so many biologists have for him guarantees that unsolicited emails requesting information are always answered if they begin with the line ... “I was a student of Bill Hamilton”. The reason I should solicit information at all is that I am deeply fascinated by what exactly people mean when they speak of his “legendary knowledge” of the natural world (TRIVERS 2000). This essay is an attempt to document some of the natural history meanderings of Bill Hamilton. Such curiosity may be justified, as my own work (on peculiar parasites of social wasps) owes everything to a natural history episode of Bill’s, which Luisa Bozzi, his partner for the last 6 years of his life, humorously related at a Social Insect Meeting in Florence, July 2000. Luisa described an old abandoned house on a hill in Tuscany set among rolling fields of olive tress. Such a property appealed to her as a retirement home for them. However, Bill was increasingly nervous and uninterested in the idea. But his interest was greatly revived when he spotted that wasps had made their nest and examining close he found not only nests but also a very unusual aggregation on the blackberry bushes (Rubus spp.) that snaked through a broken window. What was unusual was not only the inactivity of these aggregating wasps but also the fact that most harboured a particular parasite. Correctly identifying it as an insectStrepsiptera, and supposing that its presence accounted for such unusual behaviour, he set about collecting the aggregations. Discussions of domesticity gave way to science and talk of retirement to parasite manipulation of host behaviour. Luisa could but follow! She remarked that many times a walk and conversation in the Ethology Ecology & Evolution 14: 83-89, 2002

The entomopathogenic Fungi comprise a wide range of ecologically diverse species. This group of parasites can be found distributed among all fungal phyla and as well as among the ecologically similar but phylogenetically distinct Oomycetes or water molds, that belong to a different kingdom (Stramenopila). As a group, the entomopathogenic fungi and water molds parasitize a wide range of insect hosts from aquatic larvae in streams to adult insects of high canopy tropical forests. Their hosts are spread among 18 orders of insects, in all developmental stages such as: eggs, larvae, pupae, nymphs and adults exhibiting completely different ecologies. Such assortment of niches has resulted in these parasites evolving a considerable morphological diversity, resulting in enormous biodiversity, much of which remains unknown. Here we gather together a huge amount of records of these entomopathogens to comparing and describe both their morphologies and ecological traits. These findings highlight a wide range of adaptations that evolved following the evolutionary transition to infecting the most diverse and widespread animals on Earth, the insects.

In tropical forests, one of the most common relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. These fungi have the ability to penetrate the exoskeleton of the ant and to manipulate the behavior of the host, making it leave the nest and ascend understorey shrubs, to die biting onto the vegetation: hence, the term zombie-ant fungi to describe this behavioral changes on the host. It is posited that this behavioral change aids spore dispersal and thus increases the chances of infection. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe three new and host-specific species of the genus Ophiocordyceps on Camponotus ants from the central Amazonian region of Brazil which can readily be separated using classic taxonomic criteria, in particular ascospore morphology. In addition, we also employed molecular techniques to show for the first time the phylogenetic relationships between these taxa and closely related species within the Ophiocordyceps unilateralis complex, as well as with other members of the family Ophiocordycipitaceae.

Ophiocordycipitaceae is a diverse family comprising ecologically, economically, medicinally, and culturally important fungi. The family was recognized due to the polyphyly of the genus Cordyceps and the broad diversity of the mostly arthropod-pathogenic lineages of Hypocreales. The other two cordyceps-like families, Cordycipitaceae and Clavicipitaceae, will be revised taxonomically elsewhere. Historically, many species were placed in Cordyceps, but other genera have been described in this family as well, including several based on anamorphic features. Currently there are 24 generic names in use across both asexual and sexual life stages for species of Ophiocordycipitaceae. To reflect changes in Art. 59 in the International Code of Nomenclature for algae, fungi, and plants (ICN), we propose to protect and to suppress names within Ophiocordycipitaceae, and to present taxonomic revisions in the genus Tolypocladium, based on rigorous and extensively sampled molecular phylogenetic analyses. When approaching this task, we considered the principles of priority, monophyly, minimizing taxonomic revisions, and the practical utility of these fungi within the wider biological research community.

Despite the widely held position that the social insects have evolved effective ways to limit infectious disease spread, many pathogens and parasites do attack insect societies. Maintaining a disease-free nest environment is an important evolutionary feature, but since workers have to leave the nest to forage they are routinely exposed to disease. Here we show that despite effective social immunity, in which workers act collectively to reduce disease inside the nest, 100% of studied ant colonies of Camponotus rufipes in a Brazilian Rainforest were infected by the specialized fungal parasite Ophiocordyceps unilateralis s.l. Not only is disease present for all colonies but long-term dynamics over 20 months revealed disease is a permanent feature. Using 3D maps, we showed the parasite optimizes its transmission by controlling workers’ behavior to die on the doorstep of the colony, where susceptible foragers are predictable in time and space. Therefore, despite social immunity, specialized diseases of ants have evolved effective strategies to exploit insect societies.

Every level of biological organization from cells to societies require that composing units come together to form parts of a bigger unit (1). Our knowledge of how behavioral manipulating parasites change social interactions between social hosts is limited. Here we use an endoparasite to observe changes in social interactions between infected and healthy ants, using trophallaxis (liquid food exchange) and spatial data as proxies for food sharing and social segregation. We found no change in trophallaxis (p-value=0.5156). By using K-function and nearest neighbor analyses we did see a significant difference in spatial segregation on day 3 (less than 8 millimeters; p-value

Many studies have investigated how social insects behave when a parasite is introduced into their colonies. These studies have been conducted in the laboratory, and we still have a limited understanding of the dynamics of ant-parasite interactions under natural conditions. Here we consider a specialized parasite of ant societies (Ophiocordyceps camponoti-rufipedis infecting Camponotus rufipes) within a rainforest. We first established that the parasite is unable to develop to transmission stage when introduced within the host nest. Secondly, we surveyed all colonies in the studied area and recorded 100% prevalence at the colony level (all colonies were infected). Finally, we conducted a long-term detailed census of parasite pressure, by mapping the position of infected dead ants and foraging trails (future hosts) in the immediate vicinity of the colonies over 20 months. We report new dead infected ants for all the months we conducted the census – at an average of 14.5 cadavers/month/colony. Based on the low infection rate, the absence of colony collapse or complete recovery of the colonies, we suggest that this parasite represents a chronic infection in the ant societies. We also proposed a “terminal host model of transmission” that links the age-related polyethism to the persistence of a parasitic infection.

Trail-making ants lay pheromones on the substrate to define paths between foraging areas and the nest. Combined with the chemistry of these pheromone trails and the physics of evaporation, trail-laying and trail-following behaviours provide ant colonies with the quickest routes to food. In relatively uniform environments, such as that provided in many laboratory studies of trail-making ants, the quickest route is also often the shortest route. Here, we show that carpenter ants (Camponotus rufipes), in natural conditions, are able to make use of apparent obstacles in their environment to assist in finding the fastest routes to food. These ants make extensive use of fallen branches, twigs and lianas as bridges to build their trails. These bridges make trails significantly longer than their straight line equivalents across the forest floor, but we estimate that ants spend less than half the time to reach the same point, due to increased carriage speed across the bridges. We also found that these trails, mainly composed of bridges, are maintained for months, so they can be characterized as trunk trails. We suggest that pheromone-based foraging trail networks in field conditions are likely to be structured by a range of potentially complex factors but that even then, speed remains the most important consideration.

Summary Although host manipulation is likely to be costly for parasites, we still have a poor understanding of the energetic aspects underlying this strategy. It is traditionally assumed that physiological costs are inevitably associated with mechanisms evolved by parasites to induce the required changes in host behaviours. While most energetic expenditures of parasites relate primarily to bringing about the altered behaviours, manipulative parasites also have to consider the condition of their host during the manipulation. Here, we suggest that because of this trade-off, the energy required to accomplish parasite-induced behaviours may represent a key energetic constraint for parasites. Depending on the energetic expenditures specific to each type of manipulation, parasites should undergo selection to secure resources for their host to allow them to perform manipulated behaviours.

Despite the growing number of experimental studies on mechanisms of social immunity in ant societies, little is known about how social behavior relates to disease progression within the nests of ants. In fact, when empirically studying disease in ant societies, it is common to remove dead ants from experiments to confirm infection by the studied parasite. This unfortunately does not allow disease to progress within the nest as it may be assumed would happen under natural conditions. Therefore, the approach taken so far has resulted in a limited knowledge of diseases dynamics within the nest environment. Here we introduced a single infectious cadaver killed by the fungus Beauveria bassiana into small nests of the ant Camponotus castaneus. We then observed the natural progression of the disease by not removing the corpses of the ants that died following the first entry of the disease. Because some behaviors such as social isolation of sick individuals or the removal of cadavers by nestmates are considered social immune functions and thus adaptations at the colony level that reduce disease spread, we also experimentally confined some sub-colonies to one or two chamber nests to prevent the expression of such behaviors. Based on 51 small nests and survival studies in 1,003 ants we found that a single introduced infectious cadaver was able to transmit within the nest, and social immunity did not prevent the collapse of the small sub-colonies here tested. This was true whether ants did or did not have the option to remove the infectious cadaver. Therefore, we found no evidence that the typically studied social immunity behaviors can reduce disease spread in the conditions here tested.

We present the first record of parasitism of Dolichoderus bispinosus nests by Strepsiptera belonging to the family Myrmecolacidae. This becomes only the fourteenth species of ant and the fifth subfamily to be identified as a host to Strepsiptera. Of the three colonies examined all were parasitized. Prevalence of parasitism among adult ants was less than 2% in each case. However, among alate males of one colony, nearly 24% were parasitized. In conjunction with a reanalysis of previously published data we discuss the possibility that ant castes are differentially parasitized by Strepsiptera. We review the natural history of strepsipteran parasitism in ants, effects on host behaviour and incidences of parasitism in the hope of enabling detection of this parasite by myrmecologists.

Coevolution between ant colonies and their rare specialized parasites are intriguing, because lethal infections of workers may correspond to tolerable chronic diseases of colonies, but the parasite adaptations that allow stable coexistence with ants are virtually unknown. We explore the trade-offs experienced by Ophiocordyceps parasites manipulating ants into dying in nearby graveyards. We used field data from Brazil and Thailand to parameterize and fit a model for the growth rate of graveyards. We show that parasite pressure is much lower than the abundance of ant cadavers suggests and that hyperparasites often castrate Ophiocordyceps. However, once fruiting bodies become sexually mature they appear robust. Such parasite life-history traits are consistent with iteroparity--a reproductive strategy rarely considered in fungi. We discuss how tropical habitats with high biodiversity of hyperparasites and high spore mortality has likely been crucial for the evolution and maintenance of iteroparity in parasites with low dispersal potential.

Specialized parasites are expected to express complex adaptations to their hosts. Manipulation of host behavior is such an adaptation. We studied the fungus Ophiocordyceps unilateralis, a locally specialized parasite of arboreal Camponotus leonardi ants. Ant-infecting Ophiocordyceps are known to make hosts bite onto vegetation before killing them. We show that this represents a fine-tuned fungal adaptation: an extended phenotype. Dead ants were found under leaves, attached by their mandibles, on the northern side of saplings similar to 25 cm above the soil, where temperature and humidity conditions were optimal for fungal growth. Experimental relocation confirmed that parasite fitness was lower outside this manipulative zone. Host resources were rapidly colonized and further secured by extensive internal structuring. Nutritional composition analysis indicated that such structuring allows the parasite to produce a large fruiting body for spore production. Our findings suggest that the osmotrophic lifestyle of fungi may have facilitated novel exploitation strategies.

Parasite-induced alteration of host behaviour is a widespread transmission strategy among pathogens. Understanding how it works is an exciting challenge from both a mechanistic and an evolutionary perspective. In this review, we use key examples to examine the proximate mechanisms by which parasites are known to control the behaviour of their hosts. Special attention is given to the recent developments of post-genomic tools, such as proteomics, for determining the genetic basis of parasitic manipulation. We then discuss two novel perspectives on host manipulation (mafia-like strategy and exploitation of host compensatory responses), arguing that parasite-manipulated behaviours could be the result of compromises between host and parasite strategies. Such compromises may occur when collaborating with the parasite is less costly for the host in terms of fitness than is resisting parasite-induced changes. Therefore, even when changes in host behaviour benefit the parasite, the host may still play some role in the switch in host behaviour. In other words, the host does not always become part of the parasite's extended phenotype. For example, parasites that alter host behaviour appear to induce widely disseminated changes in the hosts' central nervous system, as opposed to targeted attacks on specific neural circuits. In some host-parasite systems, the change in host behaviour appears to require the active participation of the host (e.g., via host immune-neural connections). Even when the change in host behaviour results in clear fitness benefits for the parasite, these behavioural changes may sometimes be produced by the host. Changes in host behaviour that decrease the fitness costs of infection could be selected for, even if these changes also benefit the parasite.

SummaryA recent study has discovered a novel extended phenotype of a nematode which alters its ant host to resemble ripe fruit. The infected ants are in turn eaten by frugivorous birds that disperse the nematode's eggs.

International audience; Very few parasite species are directly predated but most of them inherit the predators of their host. Weexplored the behavioural response of nematomorph hairworms when their hosts are preyed upon byone of the commonest invertebrate predators in the aquatic habitat of hairworms, notonectids. The hair-wormParagordius tricuspidatuscan alter the behaviour of its terrestrial insect host (the cricketNemobius syl-vestris), causing it to jump into the water; an aquatic habitat is required for the adult free-living stage of theparasite. We predicted that hairworms whose hosts are captured by a notonectid should accelerate theiremergence to leave the host before being killed. As predicted, the emergence length of the worm was sig-nificantly shortened in cases of notonectid predation, but the exact reason of this response seems to bemore complex than expected. Indeed, experimental manipulations revealed that hairworms are remark-ably insensitive to a prolonged exposure to predator effluvia which notonectids inject into prey, so accel-erated emergence is not a protective response against digestive enzymes. We discuss other possibilities forthe accelerated exit observed, ranging from unspecific stress responses to other scenarios requiring consid-eration of the ecological context.

It is unclear why some species become successful invaders whilst others fail, and whether invasive success depends on pre-adaptations already present in the native range or on characters evolving de-novo after introduction. Ants are among the worst invasive pests, with Lasius neglectus and its rapid spread through Europe and Asia as the most recent example of a pest ant that may become a global problem. Here, we present the first integrated study on behavior, morphology, population genetics, chemical recognition and parasite load of L. neglectus and its non-invasive sister species L. turcicus. We find that L. neglectus expresses the same supercolonial syndrome as other invasive ants, a social system that is characterized by mating without dispersal and large networks of cooperating nests rather than smaller mutually hostile colonies. We conclude that the invasive success of L. neglectus relies on a combination of parasite-release following introduction and pre-adaptations in mating system, body-size, queen number and recognition efficiency that evolved long before introduction. Our results challenge the notion that supercolonial organization is an inevitable consequence of low genetic variation for chemical recognition cues in small invasive founder populations. We infer that low variation and limited volatility in cuticular hydrocarbon profiles already existed in the native range in combination with low dispersal and a highly viscous population structure. Human transport to relatively disturbed urban areas thus became the decisive factor to induce parasite release, a well established general promoter of invasiveness in non-social animals and plants, but understudied in invasive social insects.

International audience; Theoretical and experimental studies have established the dynamic nature of virulence and that, like all traits, it has evolved. Understanding parasite evolution offers a conceptual framework for diverse fields and can contribute greatly to decision-making in disease control. Recently, Grech et al. investigated the effects of host genotype-by-parasite genotype interactions on the expression of virulence in an artificial rodent-malaria system. They found that both parasite and host effects explained most of the variance in the virulence, resistance and transmission potential. These findings are a major contribution to the emerging debate on the pros and cons of a coevolutionary approach of virulence evolution; they also hold great potential for more effective control strategies.

In tropical forests, one of the most commonly encountered relationships between parasites and insects is that between the fungus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Ascomycota) and ants, especially within the tribe Camponotini. Here, we describe three newly discovered host-specific species, Ophiocordyceps camponoti-atricipis, O. camponoti-bispinosi and O. camponoti-indiani, on Camponotus ants from the central Amazonian region of Brazil, which can readily be separated using morphological traits, in particular the shape and behavior of the ascospores. DNA sequence data support inclusion of these species within the Ophiocordyceps unilateralis complex.

International audience; One of the most fascinating anti-predator responses displayed by parasites is that of hairworms (Nematomorpha). Following the ingestion of the insect host by fish or frogs, the parasitic worm is able to actively exit both its host and the gut of the predator. Using as a model the hairworm, Paragordius tricuspidatus, (parasitizing the cricket Nemobius sylvestris) and the fish predator Micropterus salmoides, we explored, with proteomics tools, the physiological basis of this anti-predator response. By examining the proteome of the parasitic worm, we detected a differential expression of 27 protein spots in those worms able to escape the predator. Peptide Mass Fingerprints of candidate protein spots suggest the existence of an intense muscular activity in escaping worms, which functions in parallel with their distinctive biology. In a second step, we attempted to determine whether the energy expended by worms to escape the predator is traded off against its reproductive potential. Remarkably, the number of offspring produced by worms having escaped a predator was not reduced compared with controls

Background Parasites that manipulate host behavior can provide prominent examples of extended phenotypes: parasite genomes controlling host behavior. Here we focus on one of the most dramatic examples of behavioral manipulation, the death grip of ants infected by Ophiocordyceps fungi. We studied the interaction between O. unilateralis s.l. and its host ant Camponotus leonardi in a Thai rainforest, where infected ants descend from their canopy nests down to understory vegetation to bite into abaxial leaf veins before dying. Host mortality is concentrated in patches (graveyards) where ants die on sapling leaves ca. 25 cm above the soil surface where conditions for parasite development are optimal. Here we address whether the sequence of ant behaviors leading to the final death grip can also be interpreted as parasite adaptations and describe some of the morphological changes inside the heads of infected workers that mediate the expression of the death grip phenotype. Results We found that infected ants behave as zombies and display predictable stereotypical behaviors of random rather than directional walking, and of repeated convulsions that make them fall down and thus precludes returning to the canopy. Transitions from erratic wandering to death grips on a leaf vein were abrupt and synchronized around solar noon. We show that the mandibles of ants penetrate deeply into vein tissue and that this is accompanied by extensive atrophy of the mandibular muscles. This lock-jaw means the ant will remain attached to the leaf after death. We further present histological data to show that a high density of single celled stages of the parasite within the head capsule of dying ants are likely to be responsible for this muscular atrophy. Conclusions Extended phenotypes in ants induced by fungal infections are a complex example of behavioral manipulation requiring coordinated changes of host behavior and morphology. Future work should address the genetic basis of such extended phenotypes.

BackgroundOphiocordyceps unilateralis (Clavicipitaceae: Hypocreales) is a fungal pathogen specific to ants of the tribe Camponotini (Formicinae: Formicidae) with a pantropical distribution. This so-called zombie or brain-manipulating fungus alters the behaviour of the ant host, causing it to die in an exposed position, typically clinging onto and biting into the adaxial surface of shrub leaves. We (HCE and DPH) are currently undertaking a worldwide survey to assess the taxonomy and ecology of this highly variable species.MethodsWe formally describe and name four new species belonging to the O. unilateralis species complex collected from remnant Atlantic rainforest in the south-eastern region (Zona da Mata) of the State of Minas Gerais, Brazil. Fully illustrated descriptions of both the asexual (anamorph) and sexual (teleomorph) stages are provided for each species. The new names are registered in Index Fungorum (registration.indexfungorum.org) and have received IF numbers. This paper is also a test case for the electronic publication of new names in mycology.ConclusionsWe are only just beginning to understand the taxonomy and ecology of the Ophiocordyceps unilateralis species complex associated with carpenter ants; macroscopically characterised by a single stalk arising from the dorsal neck region of the ant host on which the anamorph occupies the terminal region and the teleomorph occurs as lateral cushions or plates. Each of the four ant species collected--Camponotus rufipes, C. balzani, C. melanoticus and C. novogranadensis--is attacked by a distinct species of Ophiocordyceps readily separated using traditional micromorphology. The new taxa are named according to their ant host.

Udgivelsesdato: March 2009 Parasites are likely to play an important role in structuring host populations. Many adaptively manipulate host behaviour, so that the extended phenotypes of these parasites and their distributions in space and time are potentially important ecological variables. The fungus Ophiocordyceps unilateralis, which is pan-tropical in distribution, causes infected worker ants to leave their nest and die under leaves in the understory of tropical rainforests. Working in a forest dynamic plot in Southern Thailand we mapped the occurrence of these dead ants by examining every leaf in 1,360 m2 of primary rainforest. We established that high density aggregations exist (up to 26 dead ants/m2), which we coined graveyards. We further established that graveyards are patchily distributed in a landscape with no or very few O. unilateralis-killed ants. At some, but not all, spatial scales of analysis the density of dead ants correlated with temperature, humidity and vegetation cover. Remarkably, having found 2243 dead ants inside graveyards we only found 2 live ants of the principal host, ant Camponotus leonardi, suggesting that foraging host ants actively avoid graveyards. We discovered that the principal host ant builds nests in high canopy and its trails only occasionally descend to the forest floor where infection occurs. We advance the hypothesis that rare descents may be a function of limited canopy access to tree crowns and that resource profitability of such trees is potentially traded off against the risk of losing workers due to infection when forest floor trails are the only access routes. Our work underscores the need for an integrative approach that recognises multiple facets of parasitism, such as their extended phenotypes.

SummaryA new study reveals that an apparent mutualism between lycaenid caterpillars and their attendant ants may not be all it seems, as the caterpillars produce secretions that modify the brains and behavior of their attendant ants.