Paulo F. Cristaldo

Diet Segregation between Cohabiting Builder and Inquiline Termite Species.

How do termite inquilines manage to cohabit termitaria along with the termite builder species? With this in mind, we analysed one of the several strategies that inquilines could use to circumvent conflicts with their hosts, namely, the use of distinct diets. We inspected overlapping patterns for the diets of several cohabiting Neotropical termite species, as inferred from carbon and nitrogen isotopic signatures for termite individuals. Cohabitant communities from distinct termitaria presented overlapping diet spaces, indicating that they exploited similar diets at the regional scale. When such communities were split into their components, full diet segregation could be observed between builders and inquilines, at regional (environment-wide) and local (termitarium) scales. Additionally, diet segregation among inquilines themselves was also observed in the vast majority of inspected termitaria. Inquiline species distribution among termitaria was not random. Environmental-wide diet similarity, coupled with local diet segregation and deterministic inquiline distribution, could denounce interactions for feeding resources. However, inquilines and builders not sharing the same termitarium, and thus not subject to potential conflicts, still exhibited distinct diets. Moreover, the areas of the builder’s diet space and that of its inquilines did not correlate negatively. Accordingly, the diet areas of builders which hosted inquilines were in average as large as the areas of builders hosting no inquilines. Such results indicate the possibility that dietary partitioning by these cohabiting termites was not majorly driven by current interactive constraints. Rather, it seems to be a result of traits previously fixed in the evolutionary past of cohabitants.

Mutual use of trail-following chemical cues by a termite host and its inquiline.

Termite nests are often secondarily inhabited by other termite species ( = inquilines) that cohabit with the host. To understand this association, we studied the trail-following behaviour in two Neotropical species, Constrictotermes cyphergaster (Termitidae: Nasutitermitinae) and its obligatory inquiline, Inquilinitermes microcerus (Termitidae: Termitinae). Using behavioural experiments and chemical analyses, we determined that the trail-following pheromone of C. cyphergaster is made of neocembrene and (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol. Although no specific compound was identified in I. microcerus, workers were able to follow the above compounds in behavioural bioassays. Interestingly, in choice tests, C. cyphergaster prefers conspecific over heterospecific trails while I. microcerus shows the converse behaviour. In no-choice tests with whole body extracts, C. cyphergaster showed no preference for, while I. microcerus clearly avoided heterospecific trails. This seems to agree with the hypothesis that trail-following pheromones may shape the cohabitation of C. cyphergaster and I. microcerus and reinforce the idea that their cohabitation is based on conflict-avoiding strategies.

Combined foraging strategies and soldier behaviour in Nasutitermes aff. coxipoensis (Blattodea: Termitoidea: Termitidae).

A range of behavioural strategies and sensory abilities allows animals to minimize costs involved in food search. By building a network of tunnels and presenting a large number of soldiers (i.e., trophically dependent individuals), Nasutitermes spp. termites feature behaviours that imply additional costs during this process. Here we evaluated N. aff. coxipoensis foraging strategies focusing on the role of soldiers during foraging. Field experiments were carried out via nests transplantation to dune areas, and laboratory experiments evaluated termite responses to sternal gland chemical signals from workers and soldiers. N. aff. coxipoensis presented primarily nocturnal foraging. Soldiers typically initiated foraging; however, in established trails, the number of workers was always higher than that of soldiers. The number of trails remained constant over time, while the number of tunnels increased linearly over time. A higher proportion of tunnels originated in surrounding areas than directly from the nests. At observation points with tunnels, there were more stationary than walking soldiers; the opposite was true at observation points without tunnels. In mixed groups, the workers chose to follow soldier chemical signals, and in these groups, soldiers were the first to follow trails. Our results allowed us to identify a not common foraging strategy in termite species; which included the establishment of trails followed by construction of tunnels. Such foraging strategies occur predominantly at night and soldiers play a key role in the foraging process. This foraging strategy reported here seems to be employed to optimize energetic gain.

The nature of alarm communication in Constrictotermes cyphergaster (Blattodea: Termitoidea: Termitidae): the integration of chemical and vibroacoustic signals

ABSTRACT Alarm signalling is of paramount importance to communication in all social insects. In termites, vibroacoustic and chemical alarm signalling are bound to operate synergistically but have never been studied simultaneously in a single species. Here, we inspected the functional significance of both communication channels in Constrictotermes cyphergaster (Termitidae: Nasutitermitinae), confirming the hypothesis that these are not exclusive, but rather complementary processes. In natural situations, the alarm predominantly attracts soldiers, which actively search for the source of a disturbance. Laboratory testing revealed that the frontal gland of soldiers produces a rich mixture of terpenoid compounds including an alarm pheromone. Extensive testing led to identification of the alarm pheromone being composed of abundant monoterpene hydrocarbons (1S)-α-pinene and myrcene, along with a minor component, (E)-β-ocimene. The vibratory alarm signalling consists of vibratory movements evidenced as bursts; a series of beats produced predominantly by soldiers. Exposing termite groups to various mixtures containing the alarm pheromone (crushed soldier heads, frontal gland extracts, mixture of all monoterpenes, and the alarm pheromone mixture made of standards) resulted in significantly higher activity in the tested groups and also increased intensity of the vibratory alarm communication, with the responses clearly dose-dependent. Lower doses of the pheromone provoked higher numbers of vibratory signals compared to higher doses. Higher doses induced long-term running of all termites without stops necessary to perform vibratory behaviour. Surprisingly, even crushed worker heads led to low (but significant) increases in the alarm responses, suggesting that other unknown compound in the workers head is perceived and answered by termites. Our results demonstrate the existence of different alarm levels in termites, with lower levels being communicated through vibratory signals, and higher levels causing general alarm or retreat being communicated through the alarm pheromone. Summary: We inspected the functional significance of both vibroacoustic and chemical communication channels in Constrictotermes cyphergaster (Termitidae: Nasutitermitinae), confirming the hypothesis that these are not exclusive but rather complementary processes.

Allometric Scaling of Patrolling Rate and Nest Volume in Constrictotermes cyphergaster Termites: Hints on the Settlement of Inquilines.

Structural and functional traits of organisms are known to be related to the size of individuals and to the size of their colonies when they belong to one. Among such traits, propensity to inquilinism in termites is known to relate positively to colony size. Larger termitaria hold larger diversity of facultative inquilines than smaller nests, whereas obligate inquilines seem unable to settle in nests smaller than a threshold volume. Respective underlying mechanisms, however, remain hypothetical. Here we test one of such hypotheses, namely, that nest defence correlates negatively to nest volume in Constrictotermes cyphergaster termites (Termitidae: Nasutitermitinae). As a surrogate to defence, we used ‘patrolling rate’, i.e., the number of termite individuals attending per unit time an experimentally damaged spot on the outer wall of their termitaria. We found that patrolling rate decayed allometrically with increasing nest size. Conspicuously higher patrolling rates occurred in smaller nests, while conspicuously lower rates occurred in larger nests presenting volumes in the vicinity of the threshold value for the establishment of inquilinism. This could be proven adaptive for the host and guest. At younger nest age, host colonies are smaller and presumably more vulnerable and unstable. Enhanced defence rates may, hence, prevent eventual risks to hosts from inquilinism at the same time that it prevents inquilines to settle in a still unstable nest. Conversely, when colonies grow and maturate enough to stand threats, they would invest in priorities other than active defence, opening an opportunity for inquilines to settle in nests which are more suitable or less risky. Under this two-fold process, cohabitation between host and inquiline could readily stabilize.

Resource suitability modulating spatial co‐occurrence of soil‐forager termites (Blattodea: Termitoidea)

Resource can regulate animal foraging range, which in turn determines the chances of species co‐occurrence. Here, we addressed the question of whether resource determines the co‐occurrence of soil‐forager termite species (i.e. those foraging in subterranean tunnels). Eight quadrats (4 × 4 m) were marked in seven sites of Brazilian Atlantic rainforests, giving a total area sampled of 896 m2. Inside each quadrat, we measured the co‐occurrence of soil forager species and the resource suitability (N:C ratio of the soil and litter biomass). The number of records of more than one soil‐forager termite species at a single foraging spot, relative to the total number of foraging spots detected in each forest, was taken as a surrogate for spatial co‐occurrence. We tested whether termite co‐occurrence was mediated by random or nonrandom processes. Data were subjected to linear regression to test how the termite species co‐occurrence responds to resources. We compared this method with a null model analysis. Soil‐forager termites comprised 885 records, 20 species and 14 genera. From those records, 29% indicated species co‐occurrence. Co‐occurrence was not random: occurred more frequently when resource suitability was very high or very low. This result suggests an optimised use of space by termite communities.

Smells Like Home: Chemically Mediated Co-Habitation of Two Termite Species in a Single Nest

Termite nests often are referred to as the most elaborate constructions of animals. However, some termite species do not build a nest at all and instead found colonies inside the nests of other termites. Since these so-called inquilines do not need to be in direct contact with the host population, the two colonies usually live in separate parts of the nest. Adaptations of both the inquiline and its host are likely to occur to maintain the spatial exclusion and reduce the costs of potential conflicts. Among them, mutual avoidance, based on chemical cues, is expected. We investigated chemical aspects of cohabitation between Constrictotermes cavifrons (Nasutitermitinae) and its obligatory inquiline Inquilinitermes inquilinus (Termitinae). Inquiline soldiers produce in their frontal glands a blend of wax esters, consisting of the C12 alcohols (3Z)-dodec enol, (3Z,6Z)-dodecadienol, and dodecanol, esterified with different fatty acids. The C12 alcohols appear to be cleaved gradually from the wax esters, and they occur in the frontal gland, in soldier headspace, and in the walls of the inquiline part of the nest. Electrophysiological experiments revealed that (3Z)-dodecenol and (3Z,6Z)-dodecadienol are perceived by workers of both species. Bioassays indicated that inquiline soldier heads, as well as the two synthetic compounds, are attractive to conspecific workers and elicit an arresting behavior, while host soldiers and workers avoid these chemicals at biologically relevant amounts. These observations support the hypothesis that chemically mediated spatial separation of the host and the inquiline is an element of a conflict-avoidance strategy in these species.

Heterospecific detection of host alarm cues by an inquiline termite species (Blattodea: Isoptera: Termitidae)

Termite inquilines specialize on living in and feeding on a host termite nest. However, the mechanisms allowing survival of two mutually hostile populations confined to a single nest are not understood. Here we report on inquiline termites that respond to their hosts alarm cues. Upon detecting these cues, the inquilines do not join in with the hosts nest defence, but use this information for their own benefit, to escape danger. Using behavioural bioassays under laboratory conditions, we show that the obligatory inquiline Inquilinitermes microcerus (Termitidae: Termitinae) responds both to its own alarm signal and to alarm cues from its host, Constrictotermes cyphergaster (Termitidae: Nasutitermitinae). Conversely, this host responded only to its own alarm signal. Despite perceiving their hosts alarm cues, inquilines were never observed sharing nest defence with their host in experimentally damaged nests in the field. We argue that this allows inquilines not only to minimize encounters and hence conflict with their hosts, but also to use their host alarm information to escape the hosts enemies, which are also likely to be enemies of the inquilines. Our results show a new benefit that inquilines gain from the host, and we discuss the inquiline way-of-life from an evolutionary perspective, as the outcome of constraints and benefits imposed by living in host nests.

Nematode Root Herbivory in Tomato Increases Leaf Defenses and Reduces Leaf Miner Oviposition and Performance

The outcome of plant-mediated interactions among herbivores from several feeding guilds has been studied intensively. However, our understanding on the effects of nematode root herbivory on leaf miner oviposition behavior and performance remain limited. In this study, we evaluated whether Meloidogyne incognita root herbivory affects Tuta absoluta oviposition preference on Solanum lycopersicum plants and the development of the resulting offspring. To investigate the M. incognita-herbivory induced plant systemic responses that might explain the observed biological effects, we measured photosynthetic rates, leaf trypsin protease inhibitor activities, and analyzed the profile of volatiles emitted by the leaves of root-infested and non-infested plants. We found that T. absoluta females avoided laying eggs on the leaves of root-infested plants, and that root infestation negatively affected the pupation process of T. absoluta. These effects were accompanied by a strong suppression of leaf volatile emissions, a decrease in photosynthetic rates, and an increase in the activity of leaf trypsin protease inhibitors. Our study reveals that root attack by nematodes can shape leaf physiology, and thereby increases plant resistance.

Sub-lethal effects of essential oil of Lippia sidoides on drywood termite Cryptotermes brevis (Blattodea: Termitoidea)

The drywood termite Cryptotermes brevis (Walker, 1853) (Kalotermitidae) is one of the most important wood structural pest in the world. Substances from the secondary metabolism of plants (e.g., essential oils) have been considered an environmentally safer form of control for urban pests, such as termites. In the present study, we analyzed the lethal and sub-lethal effects of essential oil of Lippia sidoides and its major components on C. brevis pseudergates in two routes of exposure (contact and fumigation). The essential oil of L. sidoides and thymol were more toxic to C. brevis pseudergates when applied by contact (LD50 = 9.33 and 8.20µgmg-1, respectively) and by fumigation (LC50 = 9.10 and 23.6µLL-1, respectively). In general, treatments changed the individual and collective behaviors of C. brevis pseudergates, as well as the displacement and walking speed. The essential oil of L. sidoides and its major components showed a high potential to control C. brevis pseudergates, due to the bioactivity in the two routes of exposure and the sub-lethal effects on the behavior and walking, important activities for the cohesion of C. brevis colonies.