James F. A. Traniello

The development of immunity in a social insect: Evidence for the group facilitation of disease resistance

The extraordinary diversity and ecological success of the social insects has been attributed to their ability to cope with the rich and often infectious microbial community inhabiting their nests and feeding sites. Mechanisms of disease control used by eusocial species include antibiotic glandular secretions, mutual grooming, removal of diseased individuals from the nest, and the innate and adaptive immune responses of colony members. Here we demonstrate that after a challenge exposure to the entomopathogenic fungus Metarhizium anisopliae, dampwood termites Zootermopsis angusticollis have higher survivorship when individuals develop immunity as group members. Furthermore, termites significantly improve their ability to resist infection when they are placed in contact with previously immunized nestmates. This “social transfer” of infection resistance, a previously unrecognized mechanism of disease control in the social insects, could explain how group living may improve the survivorship of colony members despite the increased risks of pathogen transmission that can accompany sociality.

Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae)

Abstract The benefit of sociality in relation to disease susceptibility was studied in the dampwood termite Zootermopsis angusticollis. Although contact with high concentrations of fungal conidia is lethal, the survivorship of nymphs exposed to spore suspensions ranging from 6 × 106 to 2 × 108 spores/ml of the fungus Metarhizium anisopliae increased with group size. The survivorship (measured as LT50) of isolated individuals ranged from 3.0 to 4.8 days, but infected nymphs living in groups of 10 and 25 individuals survived significantly longer (5.6–8.3 and 5.6–9.1 days, respectively). In most cases, there were no significant differences in the survival distributions of the 10- and 25-termite groups. When nymphs were infected with concentrations of 7 × 101–7 × 104 spores/ml and allowed to interact with healthy nestmates, fungal infections were not contracted by the unexposed termites. Moreover, infected termites benefitted from social contact with unexposed nestmates: their survival rates were significantly higher than those of infected termites living with similarly infected nestmates. Allogrooming, which increased in frequency during and after exposure to conidia, appeared to remove potentially infectious spores from the cuticle, thus increasing termite survivorship. These results suggest that allogrooming plays a crucial role in the control of disease and its death hazard in termites. The infection-reducing advantage of group living may have been significant in the evolution of social behavior in the Isoptera.

Territoriality, Nest Dispersion,and Community Structure in Ants

The dispersion patterns of ant colonies have been reported for a variety of species having very different ecological characteristics (Pontin 1961; Yasuno 1963, 1964a,b, 1965; Brian 1964; Brian et al. 1965, 1966; Greenslade 1971; Room 1971, 1975a,b; Bernstein and Gobbel 1979; Levings and Franks 1982), and typically, spacing studies involve discussions of territoriality. Recently, Holldobler and Lumsden (1980), using a cost/ benefit approach, examined the importance of the economic defensibility of territories and its influence on the use of space and dispersion patterns. Holldobler (1974, 1976a, 1979a,b) demonstrated the relationship between resource distribution, territory shape and nest spacing. These studies also emphasize that in order to understand thoroughly territoriality and other intraand interspecific relationships, it is necessary to comprehend the role of social design in the establishment and maintenance of territory. Without such a combined approach of behavior and ecology, it is difficult to assess accurately the significance of territoriality in social species such as ants. In many studies there have been problems in the application of the term territoriality and discrepancies in the identification of territorial phenomena. Terms describing the use of foraging area such as territory and home range have been rather poorly defined and vary in meaning between authors. Territory to some authors denotes a defended area (Baroni-Urbani 1979; Holldobler 1974, 1976a; Holldober and Wilson 1977a,b; Holldobler and Lumsden 1980) whereas to others it is synonymous with home range or is casually used (Dobrzanska 1958, 1966). There are also problems with the application of information on territoriality in the interpretation of spacing patterns. For example, mathematical evidence of

Reproductive dynamics and colony structure of subterranean termites of the genus Reticulitermes (Isoptera Rhinotermitidae): a review of the evidence from behavioral, ecological, and genetic studies

(1) In subterranean termites of the genus Reticulitermes, colonies are difficult to delineate because physical nest structures are concealed or amorphous, and colony boundaries are difficult to define. The ambiguity of colony architecture and the cryptic nesting and feeding habits of these ecologically and economically important termites hinder our understanding of their population biology. We review and synthesize current information on Reticulitermes life history, reproduction, and genetics to develop an understanding of colony and population structure, and possible modes of reproductive organization. (2) To infer colony structure, we simulate several breeding systems that might be found in Reticulitermes and determine the F statistics and relatedness coefficients expected for groups of workers drawn from the simulated populations. Available field data on the distribution of worker genotypes within and among colonies are then used to distinguish between alternate hypotheses regarding population and bree...

Behavior and Ecology of Foraging in Termites

Foraging behavior has evolved in concert with termite life types, some species feeding on the wood in which they live and others harvesting food that is separate from the nest. The nutritional value of food sources appears to be critically important to colony foundation by alates as well as food selection by workers. Termite foraging is often a collective process in which groups of individuals search in organized patterns for new food sources and communicate their location by the use of sternal gland pheromones to other colony members. Division of labor between soldiers and workers and among workers is observed in the foraging activities of some rhinotermitids and in many species of higher termites. Soldiers function chiefly in the defense of workers, but may also explore new areas for food and recuit workers to newly discovered resources. Workers collect and process food, but may also defend foraging territory. The degree of caste polyethism seems to be correlated with termite ecology, and division of labor is most elaborate in fungus-growing termites such as Macrotermes. Many aspects of termite foraging, such as the measurement of task efficiency, the role of individuals and analysis of mechanisms of collective action require additional study.

Behavioural and ecological correlates of male and female parental care and reproductive success in burying beetles (Nicrophorus spp.)

Abstract Burying beetles (Coleoptera: Silphidae, Nicrophorus) from a natural population in southern New Hampshire were attracted to small carcasses which they were induced to bury into jars to rear broods. The duration of male and female parental care and their resulting reproductive success were measured by capturing departing parents and, later, their eclosing offspring. In all four species, N. orbicollis, N. sayi, N. defodiens and N. tomentosus, females provided significantly longer care than males. The principal determinant of the duration of maternal care in N. orbicollis, the focal species in this study, was carcass weight; females provided longer care on larger carcasses. Although males provided shorter care on the smallest carcasses, the duration of male care was not strongly associated with carcass weight or male or female size. Carcass weight was the major determinant of total brood weight, the best single measure of reproductive success, but offspring size was most strongly affected by the duration of maternal care. Broods begun in the first few weeks of the breeding season were heavier than later broods, perhaps due to less intense competition with flies at this time of year or brood order. First broods were significantly heavier than subsequent broods in the laboratory. The influence of behavioural and ecological factors on individual variation in parental investment and reproductive success are discussed in the context of the evolution of the roles of each parent in provisioning and guarding offspring.

Inhibition of Fungal Spore Germination by Nasutitermes: Evidence for a Possible Antiseptic Role of Soldier Defensive Secretions

The antifungal property of two of the principal components of the terpenoid frontal gland secretions of nasute termite soldiers was studied by incubating spore suspensions of the fungus Metarhizium anisopliae with α-pinene and limonene singly or in combination at different concentrations. In vitro assays showed that these substances reduced spore germination through direct and indirect (vapor) contact. To determine if the frontal gland secretions protected termites from fungal infection in vivo, the effect of M. anisopliae on the time course of survival of Nasutitermes costalis and N. nigriceps was studied by exposing termites to either a 4.3 × 107 spores/ml or a control sporeless suspension. The caste composition of experimental groups was manipulated to create mixed-caste subcolonies and monocaste groups. Relative to Coptotermes formosanus, a species that relies on the mechanical defenses of soldiers, N. costalis and N. nigriceps were less susceptible to fungal infection. Spore-exposed N. costalis and N. nigriceps termites had 1.2 times the hazard ratio of death of controls, while the hazard ratio of death of spore-exposed C. formosanus was 11.4 times that of controls. Although the lower susceptibility to infection in Nasutitermes may be explained in part by the antifungal properties of α-pinene and limonene, group composition also played a major role in the survival of spore-exposed termites. Mixed-caste and soldier monocaste groups had 3.4 and 4.7 times the hazard ratio of death, respectively, relative to the worker monocaste treatment. These results suggest that although Nasutitermes terpenoid secretions may have antifungal properties, the caste composition of groups and the social interactions of termites also play a role in determining susceptibility to fungal infection.

Inhibitory Effect of Termite Fecal Pellets on Fungal Spore Germination

The dampwood termite Zootermopsis angusticollis lines nest chambers and galleries with fecal pellets. The antifungal properties of feces were tested by recording germination rates of spores of the fungus Metarhizium anisopliae that had been incubated with various concentrations of fecal material. The presence of fecal pellet material significantly decreased the germination rates of spores relative to those of control spore solutions lacking fecal material. Spore germination rates were inversely proportional to the amount of fecal matter present in the spore–feces suspensions but were independent of incubation time. The fungistatic effect of the fecal material is virtually immediate and does not require prolonged contact with spores to inhibit germination. This mechanism of biochemical protection may reduce risks of fungal infection in termite nests.

Variation in colony structure in the subterranean termite Reticulitermes flavipes

Abstract The genetic organization of colonies of the subterranean termite Reticulitermes flavipes in two subpopulations in Massachusetts was explored using five polymorphic allozymes and double-strand conformation polymorphism (DSCP) analysis of the mitochondrial control region. Empirically obtained estimates of worker relatedness and F-statistics were compared with values generated by computer simulations of breeding schemes to make inferences about colony organization. In one study site (G), worker genotypes indicated the presence of a mixture of colonies headed by monogamous outbred primary reproductives and colonies headed by inbreeding neotenic reproductives, both colony types having limited spatial ranges. A second site (S) was dominated by several large colonies with low relatedness among nestmates. Mixed DSCP haplotypes in three colonies indicated that nestmates had descended from two or three unrelated female reproductives. Computer simulations of breeding schemes suggested that positive colony inbreeding coefficients at site S resulted from either commingling of workers from different nests or different colonies. Such an exchange of workers between nests corresponds to the multiple-site nesting lifetype of many subterranean termites and resembles colony structure in polycalic Formica ants. Our study demonstrates considerable variation in R. flavipes colony structure over a small spatial scale, including colonies headed by monogamous outbred primary reproductives, colonies containing multiple inbred neotenic reproductives and large polydomous colonies containing the progeny of two or more unrelated queens, and suggests that the number of reproductives and nestmate relatedness change with colony age and size.

Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis

Recent research has shown that low genetic variation in individuals can increase susceptibility to infection and group living may exacerbate pathogen transmission. In the eusocial diploid termites, cycles of outbreeding and inbreeding characterizing basal species can reduce genetic variation within nestmates during the life of a colony, but the relationship of genetic heterogeneity to disease resistance is poorly understood. Here we show that, one generation of inbreeding differentially affects the survivorship of isolated and grouped termites (Zootermopsis angusticollis) depending on the nature of immune challenge and treatment. Inbred and outbred isolated and grouped termites inoculated with a bacterial pathogen, exposed to a low dose of fungal pathogen or challenged with an implanted nylon monofilament had similar levels of immune defence. However, inbred grouped termites exposed to a relatively high concentration of fungal conidia had significantly greater mortality than outbred grouped termites. Inbred termites also had significantly higher cuticular microbial loads, presumably due to less effective grooming by nestmates. Genetic analyses showed that inbreeding significantly reduced heterozygosity and allelic diversity. Decreased heterozygosity thus appeared to increase disease susceptibility by affecting social behaviour or some other group-level process influencing infection control rather than affecting individual immune physiology.