The parasite's long arm: a tapeworm parasite induces behavioural changes in uninfected group members of its social host

Parasites can induce alterations in host phenotypes in order to enhance their own survival and transmission. Parasites of social insects might not only benefit from altering their individual hosts, but also from inducing changes in uninfected group members. Temnothorax nylanderi ant workers infected with the tapeworm Anomotaenia brevis are known to be chemically distinct from nest-mates and do not contribute to colony fitness, but are tolerated in their colonies and well cared for. Here, we investigated how tapeworm- infected workers affect colony aggression by manipulating their presence in ant colonies and analysing whether their absence or presence resulted in behavioural alterations in their nest-mates. We report a parasite-induced shift in colony aggression, shown by lower aggression of uninfected nest-mates from parasitized colonies towards conspecifics, potentially explaining the tolerance towards infected ants. We also demonstrate that tapeworm-infected workers showed a reduced flight response and higher survival, while their presence caused a decrease in survival of uninfected nest-mates. This anomalous behaviour of infected ants, coupled with their increased survival, could facilitate the parasites'' transmission to its definitive hosts, woodpeckers. We conclude that parasites exploiting individuals that are part of a society not only induce phenotypic changes within their individual hosts, but in uninfected group members as well.     

The energetic cost of reproductive conflicts in the ant Pachycondyla obscuricornis

In a variety of social animals, individuals can secure reproductive rights through aggressive dominance. Direct individual benefits of aggression are widely recognized, but underlying costs affecting group productivity, and thus indirect benefits, are less clear. Costs of aggressive regulation of reproduction are especially important in small social insect colonies, where individual workers could potentially dominate male production. We estimated the energetic costs associated with the regulation of worker reproduction in the ponerine ant Pachycondyla obscuricornis, using the total CO2 emission of a colony as a measure. The level of CO2 emission of 12 experimental colonies varied significantly during five periods with varying levels of aggression and egg-laying. Overall, CO2 emission increased with the degree of fighting in a colony, but was not associated with differences in egg-laying. Aggressive regulation of reproduction and the formation of a dominance hierarchy thus pose an energetic cost to the colony. Furthermore, workers reduce their work-activities immediately after experimental orphaning, giving a further cost to the colony. These costs might influence the outcome of conflicts over male production in ants. This paper presents the first quantification of energetic costs of aggressive behavior regulating reproduction in ants.     

Size–abundance relationships in Florida ant communities reveal how ants break the energetic equivalence rule

1. Ants are among the most abundant terrestrial organisms, yet little is known of how ant communities divide resources because it is difficult to measure the number of individuals in colonies and the density of colonies. 2. The body size–abundance relationships of the ants of five upland ecosystems in Florida were examined. The study tested whether abundance, energy use, and total biomass were distributed among species and body sizes as predicted by Damuth's energetic equivalence rule. Estimates of average worker body size, colony size, colony mass, and field metabolic rates were used to examine the relationships among body sizes, energy use, and total biomass. 3. Analyses revealed significant variation in energy use and did not support the energetic equivalence hypothesis. Specifically, the energy use and total standing biomass of species with large workers and colonies was much greater than smaller species. 4. These results suggest that larger species with larger colonies account for a disproportionate fraction of the total abundance and biomass of ants. A general model of resource allocation in colonies provides a possible explanation for why ants do not conform to the predictions of the energetic equivalence rule and for why ants are so abundant.     

Energetics of newly-mated queens and colony founding in the fungus-gardening ants Cyphomyrmex rimosus and Trachymyrmex septentrionalis (Hymenoptera: Formicidae)

Abstract.  The energetics of colony founding is investigated in the fungus gardening ants (Attini) Trachymyrmex septentrionalis and Cyphomyrmex rimosus . Similar to most ants, inseminated queens of these two species found nests independently unaccompanied by workers (haplometrosis). Whereas most ant founding queens seal themselves in a chamber and do not feed when producing a brood entirely from metabolic stores (claustral founding), the majority of fungus gardening ants must forage during the founding phase (semiclaustral founding). Laboratory-reared T. septentrionalis individuals comprise 84 dealate females collected after mating flights in June 2004. Twenty are immediately killed to obtain values for queen traits and another 20 after worker emergence for queen, fungus garden and worker traits. Cyphomyrmex rimosus comprise 22 dealate females collected in June 2005; ten of which are immediately killed and similarly prepared. Newly-mated T. septentrionalis queens have 25% of their dry weight as fat; whereas newly-mated C. rimosus queens contain 11% fat. These amounts are 50–75% less than most independently founding ant species. Trachymyrmex septentrionalis queens lose merely 5% of their energetic content during colony founding, whereas the total energetic content of their brood is more than three-fold the amount lost by the queen. Incipient T. septentrionalis colonies produce approximately half as much ant biomass per gram of fungus garden as do mature colonies. Similar to most ants, T. septentrionalis produces minim workers that are approximately 40% lighter than workers from mature colonies. Regardless of their size, T. septentrionalis workers contain much lower fat than do workers of claustral species. These data indicate that fungus gardening is adaptive because colonies can produce much cheaper offspring, making colony investment much lower.     

Parasite-induced fruit mimicry in a tropical canopy ant

Some parasites modify characteristics of intermediate hosts to facilitate their consumption by subsequent hosts, but examples of parasite-mediated mimicry are rare. Here we report dramatic changes in the appearance and behavior of nematode-parasitized ants such that they resemble ripe fruits in the tropical rain forest canopy. Unlike healthy ants, which are completely black, infected ants have bright red, berry-like gasters full of parasite eggs. The infected gasters are held in a conspicuous elevated position as the ants are walking, and they are easily detached from living ants, which also exhibit reduced defensive responses. This combination of changes presumably makes the infected ants attractive to frugivorous birds, which ingest the red gasters and pass the parasite eggs in their feces. The feces are collected by ants and fed to the developing brood, thus completing the cycle. This is the first documentation of parasites causing apparent fruit mimicry in an animal host to complete their life cycle.     

Energetic cost of foraging in the ant Rhytidoponera aurata in tropical Australia

Abstract. The energetic costs of foraging by the ant Rhytidoponera aurata (Roger) were investigated both in the laboratory and field. The cost of running was estimated for workers under controlled conditions in the laboratory. Ants were placed in a ring‐shaped respiration chamber, connected to a through‐flow respirometer, in which they could run freely while their speed and respiratory rates were monitored simultaneously. The energetic costs were measured for workers while running at different speeds, and the same individuals were then used to measure the additional costs of carrying loads. Loads consisted of pieces of platinum one to two times the body mass of the ant, glued to the ants' thoraxes. These were relatively small loads compared to their natural food items. The mean cost of locomotion was 166 mJ/mg/km, and the mean cost of load carriage was 179 mJ/mg/km. A field experiment was carried out in three biotypes in open forest in Northern Territory, Australia, where worker R. aurata forage only during daylight hours at air temperatures ranging from 31 to 36 °C. Food items were placed randomly within the territory of a nest, and the duration and distance of its transportation to the nest by a forager was recorded. There were no significant differences in the frequencies with which ants selected different sized food items in the range 15–165 mg, whereas items weighing 5 mg were selected less often. The relationship between the speed of running and size of a food item transported was linear but this differed in each of three types of ground vegetation recognized. The energy cost of load carriage was extremely small compared with the energetic benefit, e.g. the energy content in a 165 mg food item is equivalent to the cost of carrying it over a distance of 78 km taking 129 days under laboratory conditions. Thus, the main limiting factor in energetic terms for this species is not the retrieval of food items, but the foraging time required to find a food source.     

Hymenolepis microstoma: Effect of the mouse bile duct tapeworm on the metabolic rate of CF-1 mice

The metabolic rate of uninfected Mus musculus (CF-1 strain) at 30 C was 1.668 ± 0.032 ccO₂/g/hr (mean ± SE, n = 35). At 2 days postinfection (PI)the metabolic rate of infected mice was 2.64 ± 0.15 ccO₂/g/hr (n = 6), or 58% higher than that of uninfected control mice. Between 2 and 8 days PI there was a steady decrease in the metabolic rate of infected mice, and by Day 15 PI the metabolic rates of infected and uninfected mice were the same. Since gross histopathological changes (e.g., fibrosis of the bile duct and liver) in infected mice are not evident until Day 4 or 5 PI, the increased metabolic rate during the early stage of infection may be a direct response of the mouse to excretory (secretory) products of the developing parasite.     

Evidence of intracolony transmission of Thelohania solenopsae (Microsporidia: Thelohaniidae) in red imported fire ants (Hymenoptera: Formicidae) and the first report of spores from pupae.

Red imported fire ant, Solenopsis invicta, colonies were infected horizontally by introducing live brood (mainly larvae and pupae) infected with Thelohania solenopsae. Live, infected brood introduced into uninfected colonies were adopted and raised to adulthood instead of being executed by the recipient colony. Introductions of infected larvae with uninfected pupae, which eclose into adult worker caste fire ants, resulted in an 80% infection rate of the inoculated colonies. Infections from introductions of infected pupae with uninfected larvae resulted in a 37.5% infection of inoculated colonies. Infections were also detected in 11.6 and 3.7% of the adult worker caste ants that eclosed from uninfected large larvae and pupae, respectively, that were held with infected adult workers. Microscopic examination of infected brood revealed sporoblasts and large numbers of spores of T. solenopsae in S. invicta pupae.     

Exoskeletal thinning in Cephalotes atratus ants (Hymenoptera: Formicidae) parasitized by Myrmeconema neotropicum (Nematoda: Tetradonematidae)

Some parasites modify the color of their arthropod hosts, presumably to facilitate transmission to a new host. Mechanisms for such changes often are unknown, but altered exoskeletal color in adult insects typically occurs via structural modifications or redistribution of pigments. Here, we examine the cuticle structure of workers of the Neotropical canopy ant Cephalotes atratus infected with the nematode Myrmeconema neotropicum. We hypothesized that the conspicuous red color of the gaster (the globular posterior body region) of infected ants results from structural changes, specifically localized exoskeletal thinning. We used scanning electron microscopy to quantify the thickness of gaster cuticle in healthy and infected ants. For comparison, we also measured the cuticle thickness of the head of each ant, which is black in both infected and healthy individuals. The gaster cuticle was 23% thinner in infected ants (average ±SE: 14.8 ± 1.02 μm) versus healthy ants (19.2 ± 0.65 μm) after correcting for body size. In contrast, the thickness of the head exoskeleton was similar among groups. We conclude that parasite-induced thinning of the exoskeleton is associated with the red color of the gaster. Other mechanisms, including translocation or leaching of melanin (by the ant or the parasite, respectively) may operate in concert with thinning to effect the color change, and would be an appropriate extension of this research.     

Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers

Parasites by drawing nutrition from their hosts can exert an energetic stress on them. Honeybee foragers with their high metabolic demand due to flight are especially prone to such a stress when they are infected. We hypothesized that infection by the microsporidian gut parasite Nosema ceranae can lower the hemolymph sugar level of an individual forager and uncouple its energetic state from its normally tight correlation with the colony energetic state. We support our hypothesis by showing that free-flying foragers that are infected have lower trehalose levels than uninfected ones but the two do not differ in their trehalose levels when fed until satiation. The trehalose level of infected bees was also found to decline at a faster rate while their glucose level is maintained at a quantity comparable to uninfected bees. These results suggest that infected foragers have lower flying ability and the intriguing possibility that the carbohydrate levels of an individual bee can act as a modulator of its foraging behavior, independent of social cues such as colony demand for nectar. We discuss the importance of such pathophysiological changes on foraging behavior in the context of the recently observed colony collapses.     

Timing of dispersal: effect of ants on aphids

Mutualists can affect many life history traits of their partners, but it is unclear how this translates into population dynamics of the latter. Ant–aphid associations are ideal for studying this question, as ants affect aphids, both positively (e.g., protection against natural enemies) and negatively (e.g., reduction of potential growth rates). The unresolved question is whether these effects, which have been observed at the level of individuals and under controlled environmental conditions, have consequences at the population level. On estimating aerial aphid populations by using weekly suction trap data spanning up to 22 years from different locations in France, we show that in ant-attended aphid species long-distance dispersal occurs significantly later, but that the year-to-year changes in the peak number of migrants are not significantly lower than for non-attended aphids. Host alternation had the same retarding effect on dispersal as ant attendance. We discuss the delay in the timing of dispersal in ant-attended aphids, and potential costs that arise in mutualistic systems.     

Neotyphodium endophytes in grasses: deterrents or promoters of herbivory by leaf-cutting ants?

Endophytic fungi, particularly in the genus Neotyphodium, are thought to interact mutualistically with host grasses primarily by deterring herbivores and pathogens via production of alkaloidal mycotoxins. Little is known, however, about how these endophytes interact with host plants and herbivores outside the realm of agronomic forage grasses, such as tall fescue, and their livestock grazers or invertebrate pest herbivores. We tested the effects of Neotyphodium inhabiting introduced tall fescue and native Arizona fescue on preference, survival, and performance of the leaf-cutting ant, Acromyrmex versicolor, an important generalist herbivore in the southwestern United States. In a choice experiment, we determined preferences of foraging queens and workers for infected and uninfected tall fescue and Arizona fescue. In a no-choice experiment, we determined queen survival, worker production, and size of fungal gardens for foundress queens reared on diets of infected and uninfected tall fescue and Arizona fescue. Foraging workers and queens did not significantly prefer either uninfected tall fescue or Arizona fescue relative to infected grasses, although ants tended to harvest more uninfected than infected tall fescue and more infected than uninfected Arizona fescue. Queen survivorship and length of survival was greater on uninfected tall fescue, uninfected Arizona fescue, and infected Arizona fescue than on infected tall fescue or the standard diet of palo verde and mesquite leaves. No queens survived beyond 6 weeks of the study when fed the infected tall fescue diet, in contrast to the effects of the other diets. Likewise, worker production was much lower and fungal garden size much smaller on infected tall fescue than in all other treatments, including the standard diet. In general, ant colonies survived and performed better on uninfected tall fescue and infected and uninfected Arizona fescue than standard diets of palo verde and mesquite leaves. The interaction of Neotyphodium with its host grasses is highly variable and these endophytes may increase, not alter, or even decrease resistance to herbivores. The direction of the interaction depends on host and fungal genotype, herbivore species, and environmental factors. The presence of endophytes in most, if not all, host plants suggests that endophytes may alter foraging patterns, performance, and survival of herbivores, such as leaf-cutting ants, but not always in ways that increase host plant fitness. Received: 27 October 1998 / Accepted: 19 October 1998     

Nonequilibrium dynamics of social groups: insights from foraging Argentine ants

Summary We studied disturbance patterns in groups of feeding Argentine ants, Linepithema humile. All disturbances were caused by the ants themselves, without application of exogenous disturbances. The overall pattern, which consisted of a power law distribution of disturbance avalanche sizes, each of which was initiated by a single wandering ant, is similar to patterns characteristic of self-organized critical systems. In addition, we observed variation among individuals in response to disturbance according to their level of satiation. Ants with distended gasters (indicative of volume of food uptake) resumed feeding less rapidly than their thinner counterparts, and were more likely to leave food sources altogether. Although these disturbances reduce food collection because feeding ants are interrupted, they are minimal and may enable ant groups to balance collectively the advantage of rapid alarm communication with the costs of interrupted foraging from trivial disturbances.Received 18 September 2003; revised 21 November 2003; accepted 4 December 2003.     

红火蚁入侵对棉花粉蚧近距离扩散的促进作用

[背景]红火蚁与棉花粉蚧入侵到同一地区,因侵入生境重叠而相遇,进而产生互惠关系。这种互惠关系对红火蚁、棉花粉蚧的生存、扩散传播、入侵的意义和作用规律、机制等是需要解释的生态学问题。[方法]采用田问试验生态学的方法,通过迁移红火蚁蚁巢、向扶桑上接粉蚧等观察研究了红火蚁入侵对棉花粉蚧近距离扩散的影响。[结果]随着离蚁巢距离的增大,扶桑上工蚁数量逐渐减少,距离为1．0、2．0m时数量较多;发生该蚁区域距蚁巢2．0、3．0m扶桑感染粉蚧比率（75％、45％）显著高于无红火蚁区（25％、10％）,其感染比率与工蚁数量呈显著正相关,符合方程Y=0．0042X＋0．1992。[结论与意义]红火蚁入侵促进了棉花粉蚧的近距离扩散,扩散范围在2—3m。研究结果可为深入了解红火蚁与棉花粉蚧协同入侵规律等提供支持。     

When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants

Most studies aiming to determine the beneficial effect of ants on plants simply consider the effects of the presence or exclusion of ants on plant yield. This approach is often inadequate, however, as ants interact with both non-tended herbivores and tended Homoptera. Moreover, the interaction with these groups of organisms is dependent on ant density, and these functional relationships are likely to be non-linear. A model is presented here that segregates plant herbivores into two categories depending on the sign of their numerical response to ants (myrmecophiles increase with ants, non-tended herbivores decline). The changes in these two components of herbivores with increasing ant density and the resulting implications for ant-plant mutualisms are considered. It emerges that a wide range of ant densities needs to be considered as the interaction sign (mutualism or parasitism) and strength is likely to change with ant density. The model is used to interpret the results of an experimental study that varied levels of Aphis fabae infestation and Lasius niger ant attendance on Vicia faba bean plants. Increasing ant density consistently reduced plant fitness and thus, in this location, the interaction between the ants and the plant can be considered parasitic. In the Vicia faba system, these costs of ants are unlikely to be offset by other beneficial agents (e.g., parasitoids), which also visit extrafloral nectaries.     

Plant defense, herbivory, and the growth of Cordia alliodora trees and their symbiotic Azteca ant colonies

The effects of herbivory on plant fitness are integrated over a plant??s lifetime, mediated by ontogenetic changes in plant defense, tolerance, and herbivore pressure. In symbiotic ant?Cplant mutualisms, plants provide nesting space and food for ants, and ants defend plants against herbivores. The benefit to the plant of sustaining the growth of symbiotic ant colonies depends on whether defense by the growing ant colony outpaces the plant??s growth in defendable area and associated herbivore pressure. These relationships were investigated in the symbiotic mutualism between Cordia alliodora trees and Azteca pittieri ants in a Mexican tropical dry forest. As ant colonies grew, worker production remained constant relative to ant-colony size. As trees grew, leaf production increased relative to tree size. Moreover, larger trees hosted lower densities of ants, suggesting that ant-colony growth did not keep pace with tree growth. On leaves with ants experimentally excluded, herbivory per unit leaf area increased exponentially with tree size, indicating that larger trees experienced higher herbivore pressure per leaf area than smaller trees. Even with ant defense, herbivory increased with tree size. Therefore, although larger trees had larger ant colonies, ant density was lower in larger trees, and the ant colonies did not provide sufficient defense to compensate for the higher herbivore pressure in larger trees. These results suggest that in this system the tree can decrease herbivory by promoting ant-colony growth, i.e., sustaining space and food investment in ants, as long as the tree continues to grow.     

Changes in the lipid class and proximate compositions of coho salmon (Oncorhynchus kisutch) smolts infected with the nematode parasite Philonema agubernaculum

Coho salmon (Oncorhynchus kisutch) smolts infected with the nematode Philonema agubernaculum had 36% lower mean lipid content (1.4%) than nonparasitized coho salmon (2.2%) harvested simultaneously from the same outmigration. Lengths, weights, and condition factors, as well as protein and moisture content, did not differ significantly between the two groups. Lipid class compositions differed significantly between the parasitized and nonparasitized fish. None of the nematode-infected fish contained detectable triacylglycerols (TAG) or monoacylglycerols (MAG). In contrast, mean TAG and MAG contents of the nonparasitized fish totaled 5.5% of the extracted lipid. Infected smolts had lower cholesterol contents than did uninfected coho (17% for infected, 33% for uninfected). Parasitized fish had significantly higher levels of free fatty acids (mean of 57% for parasitized vs. 35% for nonparasitized) as well as the phospholipids phosphatidylethanolamine (PE) and phosphatidylcholine (PC). However, the PC/PE ratios for infected and noninfected coho did not differ significantly (2.2 for infected vs. 2.0 for uninfected). These differences suggest that the parasitic nematodes are either harvesting storage energy directly from the coho or are placing additional energetic demands on the fish to cope with the infection.     

<Emphasis Type="Italic">Myrmeconema neotropicum</Emphasis> n. g., n. sp., a new tetradonematid nematode parasitising South American populations of <Emphasis Type="Italic">Cephalotes atratus</Emphasis> (Hymenoptera: Formicidae), with the discovery of an apparent parasite-induced host morph

A new genus and species of tetradonematid nematode, Myrmeconema neotropicum n. g., n. sp., is described from larval, pupal and adult stages of Cephalotes atratus L. (Hymenoptera: Formicidae) in Peru and Panama. Diagnostic characters of the new genus include: males and females subequal in size; cuticle with minute annulations; six cephalic papillae; stylet present in all stages; stichocytes absent; trophosome degenerate; three penetration glands; gonads paired and opposite; vulva in mid-body region; single spicule; genital papillae absent; adult tails rounded; infective juveniles moult once in egg; and adults of both sexes remain in the host throughout their development. As the female nematodes mature inside the worker ants, the host gasters change colour from black to red.     

Ant‐following and the prevalence of blood parasites in birds of African rainforests

Blood parasites are widespread in birds, several are pathogenic and may affect the fitness of their hosts, and their evolution. By reanalyzing recently published data I show that parts of the variation in prevalences of parasites in the blood of African rainforest birds and the occurrence of similar or same parasite haplotypes in rather unrelated birds are well understood when considering the ecological aspects of foraging of some of these birds. Specialized ant‐following birds, which regularly follow the massive swarm raids of army ants and feed on insects flushed by the ants, have higher prevalences of nematode microfilariae (~10×), Trypanosoma (~10×), and Plasmodium parasites (~2×) and a much higher probability of infection with multiple parasites than other birds. Moreover, birds regularly attending army ant swarms share identical Trypanosoma haplotypes and show genetically similar microfilariae haplotypes. I conclude that ant‐following increases the probability of birds to get infected with blood parasites and may facilitate the switch of a parasite species from one host species to another. The costs of higher parasite intensities involved when specializing on following ant swarms may have influenced the evolution of foraging behaviour in birds of African rainforests and may help to explain the relatively low number of specialized ant‐following bird species on the African continent.     

Alloethic efficiency in the patrolling networks of a polymorphic ant,Tapinoma nigerrimum (hymenoptera: Formicidae)

This study analyses some aspects of the role of alloethism in the networks of patrolling workers of a polymorphic ant species (Tapinoma nigerrimum) in the nest surroundings. We focus on the analysis of movement and distribution patterns of different-sized individuals, and their relationship to the potential transfer of information between each other via contacts during patrolling activities. Our results suggest that small workers are potentially more efficient in these kind of activities (information discovery and transfer), because they contact each other more than could be expected by a random process based on their proportions and, also, because their deduced energetic expenditure per unit of information found or transferred is lower than that of large workers. These differences in the contacts between patrolling ants for small and large workers cannot be explained by their movement patterns (velocity, time spend in movement, turning angles), which do not differ between both groups but, rather, seem to be a consequence of their resulting distribution patterns (overdispersed for large ants and random for small ones).