Papers by Ana Maria Costa Leonardo
Arthropod Structure & Development
Entomologia Generalis, 1991
UNIV ESTADUAL PAULISTA JULIA MESQUITA FILHO,INST BIOCIENCIAS RIO CLARO,DEPT BIOL,BR-13500 RIO CLA... more UNIV ESTADUAL PAULISTA JULIA MESQUITA FILHO,INST BIOCIENCIAS RIO CLARO,DEPT BIOL,BR-13500 RIO CLARO,SP,BRAZIL
Insects, 2019
Coptotermes gestroi is a subterranean termite with colonies generally headed by a pair of primary... more Coptotermes gestroi is a subterranean termite with colonies generally headed by a pair of primary reproductives, although neotenics may occur. In this study, the male reproductive system was compared during different life stages of nymphs, alates, neotenic reproductives, and kings of C. gestroi, focusing on the modifications of this system along the maturation of these individuals. The structure of the male reproductive system follows the pattern described for insects, although C. gestroi males do not exhibit conspicuous penises and differentiated accessory glands. In kings, each testis consisted of about seven lobes, significantly increased in size as compared to younger males. The spermatogenesis begins in third-instar nymphs, which already presented spermatozoa in the testes. The seminal vesicles are individualized in C. gestroi and have a secretory distal portion and a proximal portion with a role in spermatozoa storage. The secretion of the seminal vesicles is strongly periodic...
A subfamília Apicotermitinae possui 49 gêneros distribuídos entre a África, Neotrópica e região O... more A subfamília Apicotermitinae possui 49 gêneros distribuídos entre a África, Neotrópica e região Oriental. Na<br> Neotrópica, estes cupins não apresentam soldados e o desenvolvimento de castas é pouco conhecido. A linhagem<br> áptera, ou seja, dos operários, é precedida por dois instares larvais a partir do ovo. Cupins do gênero<br> \textit{Ruptitermes} forrageiam na superfície do solo e possuem órgãos deiscentes associados ao comportamento<br> defensivo suicida. No presente estudo, foi investigada a ocorrência de dimorfismo em operários de \textit<br> {Ruptitermes pitan}, visando contribuir para o conhecimento básico da biologia da espécie. Para diferenciar os<br> operários, foi realizada uma análise morfométrica da cápsula cefálica (comprimento e largura) e da tíbia<br> anterior esquerda (comprimento) de 40 operários provenientes de duas colônias, fixados em FAA (álcool<br> absoluto, ácido acético e formaldeído na proporção 3:1:1), se...
<b>Copyright information:</b>Taken from "Neotenic formation in laboratory coloni... more <b>Copyright information:</b>Taken from "Neotenic formation in laboratory colonies of the termite after orphaning"Journal of Insect Science 2004;4():-.Published online 8 Apr 2004PMCID:PMC528870.Copyright © 2004. Open access; copyright is maintained by the authors. Neo: neotenics; N1: 1 nymph instar; N2: 2 nymph instar; N3: 3 nymph instar; N4: 4 nymph instar; N5: 5 nymph instar; N6: 6 nymph instar.
Gregarinas parasitas são comuns em invertebrados, principalmente em insetos. Estes protozoários a... more Gregarinas parasitas são comuns em invertebrados, principalmente em insetos. Estes protozoários apresentam um ciclo de vida com um estágio endógeno, no interior do corpo do inseto e um estágio exógeno, relacionado a condições ambientais externas. Infecções por gregarinas ocorrem quando insetos ingerem acidentalmente oocistos (cistos maduros), os quais estabelecem a infecção via intestino. Gregarinas já foram descritas no intestino e na hemocele de operários de várias espécies de cupins, e embora estes protozoários não matem estes insetos, aceita-se que eles diminuem a longevidade dos mesmos. \textit{Ruptitermes pitan} e \textit{Ruptitermes reconditus} são cupins sem soldados que possuem ninhos subterrâneos e forrageiam em aberto na superfície do solo. Estes cupins alimentam-se de folhas da serrapilheira, sendo que \textit{R. reconditus} armazena o alimento picado no ninho, enquanto para \textit{R. pitan} este tipo de informação é desconhecida. Operários forrageiros de ambas as espéc...
The termite Coptotermes gestroi (Wasmann 1896) (Rhinotermitidae: Coptotermitinae) is an exotic sp... more The termite Coptotermes gestroi (Wasmann 1896) (Rhinotermitidae: Coptotermitinae) is an exotic species in Brazil and information concerning its reproductive developmental biology is scarce. We induced the formation of neotenics in laboratory colonies through orphaning experiments. Orphaning experiments were conducted in three-year old colonies of C. gestroi kept under laboratory conditions. After three months, eight nymphoid neotenics were observed in one colony after queen removal. Histological analysis showed that these neotenics were non-functional. The results suggest that these individuals may have arisen from the first nymphal instar (N1) or from an early N1 instar after one or two larval moults. Neotenics also were recorded on two incipient colonies of C. gestroi that lost the queen naturally.
Proceedings of The 1st International Electronic Conference on Entomology, 2021
Colleterial glands are female accessory glands occurring in several insect lineages and may displ... more Colleterial glands are female accessory glands occurring in several insect lineages and may display different functions. Within Dictyoptera, they synthesize compounds present in the ootheca of cockroaches and mantises. However, their morphology and secretory activity in Isoptera have been poorly investigated hitherto. Here, we conducted a morphological and histochemical analysis on these structures in different-aged females of Coptotermes gestroi. Thus, colleterial glands were isolated from 2-d-old (non-egg-laying) and 80-d-old (egg-laying) queens, and photographed for posterior description. Isolated abdomens from alate females (non-egg-laying) and 4-yr-old queens (egg-laying) were processed for routine histology, and cross-sections of the colleterial glands were measured to compare epithelium height. Xilydine-Ponceau and PAS histochemical tests were applied for identification of total proteins and polysaccharides, respectively. Colleterial glands are composed of anterior and posterior glands, which are distally ramified but discharge in a common basal trunk. The anterior gland was always longer than the posterior one, although the latter structure was thicker than the former. Histological sections showed colleterial glands poorly developed in alate females, while they were well-developed in 4-yr-old queens. The epithelium height of both glands increased significantly in egg-laying-queens (P<0.0001, t test). Histochemical analysis showed that glycoproteinaceous secretion occurred only in the lumen of the posterior gland in 4yr-old queens, while it was absent in the lumen of their anterior gland, as well as in the lumen of both glands in alate females. Results suggest a chemical modification in the secretion of the colleterial glands during the queen life, especially associated with the oviposition process.
Intercolonial aggression is being used to delimit foraging territory in termite species of subter... more Intercolonial aggression is being used to delimit foraging territory in termite species of subterranean termites. The advance of the introduced pest termite Coptotermes havilandi Holmgren in the interior of Sao Paulo State is increasing its economic impact as well as its interspecific and intraspecific competition in Brazil. In order to evaluate the intraspecific agonism among different colonies collected in urban areas of Sao Paulo State were set up a series of preliminary bioassays. Different combination of nestmates from field colonies of C. havilandi of Rio Claro city showed lack of agonistic behavior. Nevertheless, encounters among individuals from Sao Paulo and Rio Claro cities showed agonistic behaviors. These preliminary results suggest that caution should be taken in using intercolonial aggression to delimit the foraging territory of C. havilandi colonies in Sao Paulo State.
Lignocellulose digestion in termites is achieved through the functional synergy between gut symbi... more Lignocellulose digestion in termites is achieved through the functional synergy between gut symbionts and host enzymes. However, some species have evolved additional associations with nest microorganisms that collaborate in the decomposition of plant biomass. In a previous study, we determined that plant material packed with feces inside the nests of Cornitermes cumulans (Syntermitinae) harbors a distinct microbial assemblage. These food nodules also showed a high hemicellulolytic activity, possibly acting as an external place for complementary lignocellulose digestion. In this study, we used a combination of ITS sequence analysis, metagenomics, and metatranscriptomics to investigate the presence and differential expression of genes coding for carbohydrate-active enzymes (CAZy) in the food nodules and the gut of workers and soldiers. Our results confirm that food nodules express a distinct set of CAZy genes suggesting that stored plant material is initially decomposed by enzymes tha...
Salivary glands are omnipresent in termites and occur in all developmental stages and castes. The... more Salivary glands are omnipresent in termites and occur in all developmental stages and castes. They function to produce, store, and secrete compounds, ranging from a feeding function to defensive mechanisms. Here, we provide a complete morphological overview of the salivary glands in the soldierless species Ruptitermes reconditus and R. xanthochiton, and the first proteomic profile of the salivary glands in a Neotropical Apicotermitinae representative, R. reconditus. Salivary glands from both species were composed of several acini, roughly spherical structures composed of two types of central cells (type I and II) and peripheral parietal cells, as well as transporting ducts and two salivary reservoirs. Central cells were richly supplied with electron-lucent secretory vesicles and rough endoplasmic reticulum, a feature of protein-secreting cells. Parietal cells of Ruptitermes spp. had conspicuous characteristics such as electron-lucent secretory vesicles surrounded by mitochondria and...
Microscopy and Microanalysis, 2020
Suicidal behavior in termite workers is an extreme defensive strategy, probably a consequence of ... more Suicidal behavior in termite workers is an extreme defensive strategy, probably a consequence of having a low number of soldiers available in the colony and there being high predation from enemies. We investigated the suicidal mechanism in workers of the Neotropical termite Neocapritermes opacus, which involves salivary gland autothysis followed by body cuticle rupture and the release of a defensive secretion. Autothysis was triggered by a physical stimulus such as a soldier bite that causes the protrusion of the salivary acini, burst reservoirs, and foregut. Histochemical and ultrastructural analyses showed salivary acini composed of peripheral parietal cells and two types of central cells, types I and II. Type I cells are filled with large electron-lucent secretory vesicles, which reacted positively to bromophenol blue and xylidine-Ponceau tests, indicating the occurrence of proteins. Type II cells are elongated and display smaller apical secretory vesicles. Parietal cells present...
Zoologischer Anzeiger, 2020
Abstract Neocapritermes opacus is a Neotropical termite, which feeds on a variety of food sources... more Abstract Neocapritermes opacus is a Neotropical termite, which feeds on a variety of food sources, including highly decayed wood and humus. Similar to many Termitidae, this species contains a mixed segment in the intestine, an anatomic distinct region composed of both mesenteric and proctodeal tissues. In Neocapritermes spp., a pair of intestinal protrusions referred to as mesenteric sacs are associated with the mixed segment. In the present study, with the aid of histological and scanning microscopy techniques, we provide a detailed anatomical and histological analyses of the mesenteric sacs in N. opacus workers. The results showed that the paired sacs are contiguous with the mesenteric component of the mixed segment and open into the ectoperitrophic space. The wall of the sacs is an epithelium composed of two types of cells (regenerative and principal) and musculature. The regenerative cells are located at the epithelium base and organized in regenerative crypts, while the principal cells are columnar and enfold the lumen of the sacs. Brush border was observed in the principal cell apex, aligned closely to rod-like bacteria. Secretory activity was observed in the principal cells and vesicles cast from them toward the sacs lumen, probably result of an apocrine activity. The sac epithelium was of mesenteric affiliation but differed from the intestinal midgut. The proctodeal epithelium was markedly different. Although some studies have been interpreted the mesenteric sacs as Malpighian nodules or Malpighian sacs, our results support that these structures are morphologically distinct and that the occurrence of mesenteric sacs is a synapomorphy for Neocapritermes. The precise function of the mesenteric sacs in termite digestion remains unclear; therefore, further investigations should carefully consider their secretory activity and symbiont population, aiming to understand their development and maintenance among these Neotropical species.
Journal of Proteomics, 2019
Termite soldiers constitute the defensive frontline of the colonies, despite workers also perform... more Termite soldiers constitute the defensive frontline of the colonies, despite workers also perform such tasks, especially within the Neotropical Apicotermitinae, in which all species are soldierless. Workers of the genus Ruptitermes display an extreme form of defense, characterized by body rupture and release of a sticky secretion. Previous observations suggested that such behavior may be advantageous against enemies, but the chemical composition of this secretion has been neglected. Here we firstly provide the proteomic profile of the defensive secretion of Ruptitermes reconditus and Ruptitermes pitan workers. Additionally, the mechanisms of action of this behavior was evaluated through different bioassays. A total of 446 proteins were identified in R. reconditus and 391 proteins in R. pitan, which were classified into: toxins, defensins and proteolytic enzymes; sticky components/ alarm communication; proteins related to detoxification processes; proteins involved in folding/conformation and post-translational modifications; housekeeping proteins; and uncharacterized/hypothetical proteins. According to the bioassays, the self-sacrifice is triggered by a physical stimulus, and the defensive secretion may cause immobility and death of the opponents. Assuming that termites are abundant in the tropics and therefore exposed to predators, suicidal behaviors seem to be advantageous, since the loss of an individual benefit the whole colony. SIGNIFICANCE: Although recent studies have reported the biochemical composition of different weapons in soldiered species of termites, such efforts had not been applied to sordierless taxa up until now. Thus, this is the first report of the defensive mechanisms in soldierless termite species based on proteomic analysis. The diversity of compounds, which included toxin-like and mucin-like proteins, reflect the mechanisms of action of the defensive secretion released by termite workers, which may cause immobility and death of the opponents. Our findings may contribute to the knowledge regarding the development of defensive strategies in termites, especially in groups which lost the soldier caste during the evolution.
Zoology, 2019
Social insects display a range of sophisticated behaviors to deal with cadavers, which together a... more Social insects display a range of sophisticated behaviors to deal with cadavers, which together act to guarantee the health and social homeostasis of their colonies. In termites, cadaver management involves an entire repertoire of activities, such as antennation, grooming, retreat, alarm and agonistic behaviors. We performed different bioassays to evaluate whether postmortem-age, origin and caste of a cadaver influence the behavior of Coptotermes gestroi. Quantitative analyses of corpse management behaviors indicated that C. gestroi is able to discriminate the origin and caste of cadavers. Cadavers of worker nestmates were preferentially cannibalized while corpses of alien workers were buried. In addition, soldiers that had been dead for 24hours were buried while freshly dead soldiers were either buried, consumed or ignored, indicating a plastic behavioral response that depends on postmortem age. Corpse consumption is an important component of corpse management repertoire because this process eliminates contaminant and enables nutrient recycling. The physical isolation of the termite corpse through burial after grooming also helps to prevent other colony members from contacting the cadaver, further mitigating against the potential spread of disease.
Insect Science, 2019
Termite colonies are usually headed by primary reproductives, which establish nests during the sw... more Termite colonies are usually headed by primary reproductives, which establish nests during the swarming season. However, secondary reproductives may develop in some species and become supplementary or replacement breeders, extending colony lifespan. Here we investigate the developmental origin, fecundity and genetic characterization of ergatoid reproductives in the Neotropical termite Nasutitermes aquilinus (Holmgren), using morphometrical and histological techniques, five microsatellite loci and the COI mitochondrial DNA. Twelve measurements performed on 208 apterous individuals of N. aquilinus revealed 10 groups, including ergatoid females, which developed from major workers through two successive molts, and were characterized by the presence of imaginal features such as eyes and wing buds. The differentiation of these features was correlated to physogastric development in these ergatoids. Histology revealed oocytes in all maturation stages in worker-derived reproductives of N. aquilinus, presence of nonflagellate spermatozoa inside the spermatheca, and royal fat body. Thus, ergatoid reproductives were reproductively functional. According to the genotypes of 221 individuals from 11 nests, and mitochondrial haplotypes of 43 ergatoids, 73% of the colonies were simple families, whereas 27% were extended families. Despite the occurrence of related reproductives, low inbreeding rates were detected within and among colonies. Such values could be explained given that sib mating itself cannot result in a higher inbreeding rate but depend on several factors discussed in detail. This is the first study to investigate the genetic structure of termite colonies influenced by the development of ergatoids, and further investigations are encouraged to understand the influence of these reproductives on colony lifespan.
Current Microbiology, 2018
The evolution of the symbiotic association with microbes allowed termites to decompose ingested l... more The evolution of the symbiotic association with microbes allowed termites to decompose ingested lignocellulose from plantderived substrates, including herbivore dung and soil humus. Representatives of the Syntermitinae (Termitidae) range in their feeding habits from wood and litter-feeding to humus-feeding species. However, only limited information is available about their feeding ecology and associated microbial communities. Here we conducted a study of the microbial communities associated to the termite Procornitermes araujoi using Illumina sequencing of the 16S and ITS rRNA genes. This species has been previously included in different feeding guilds. However, most aspects of its feeding ecology are unknown, especially those associated to its symbiotic microbiota. Our results showed that the microbial communities of termite guts and nest substrates of P. araujoi differed significantly for bacteria and fungi. Firmicutes dominated the bacterial gut community of both workers and soldiers, whereas Actinobacteria was found in higher prevalence in the nest walls. Sordariomycetes was the most abundant fungal class in both gut and nest samples and distinguish P. araujoi from the grass/litter feeding Cornitermes cumulans. Our results also showed that diversity of gut bacteria were higher in P. araujoi and Silvestritermes euamignathus than in the grass/litter feeders (C. cumulans and Syntermes dirus), that could indicate an adaptation of the microbial community of polyphagous termites to the higher complexity of their diets.
Protoplasma, 2019
Termites are eusocial cockroaches, which have received great attention due to their diversity of ... more Termites are eusocial cockroaches, which have received great attention due to their diversity of reproductive strategies. Although these novelties allow new interpretations concerning the mating biology of these insects, studies highlighting the structure of the reproductive system are limited to some termite lineages. Here we provide the first comparative analysis of the reproductive system of a drywood termite, using different aged males of Cryptotermes brevis as models. This species represents an important structural pest in tropical regions, and most aspects of its reproductive biology remain unknown, especially on males. The reproductive apparatus of C. brevis is equipped with paired testes, composed of seven testicular lobes, in which developing spermatozoa are located. The basal portion of the lobes connects to the vasa deferentia and transport spermatozoa to a pair of enlarged chambers, the seminal vesicles. These structures join in a median ejaculatory duct, which opens to the external region through a retractile penis. Spermatozoa were observed in all C. brevis males, exhibiting elongated morphology and measuring about 10 μm in length/4 μm in width. Compared with last-instar nymphs and alates, functional kings showed enlarged testes and seminal vesicles, as well as an intense secretory activity towards the lumen of the latter structures. Histochemical tests evidenced strongly PAS and xylidine Ponceau positive reactions of the secretion only in functional kings, indicating the occurrence of glycoproteins. Thus, we suggest that morphophysiological changes establish during the maturation of the reproductive system in C. brevis.
Journal of Applied Entomology, 2018
Currently, the control of termites is mainly carried out with the use of chemical pesticides, whi... more Currently, the control of termites is mainly carried out with the use of chemical pesticides, which although effective, pose risks to the environment and to human beings. An alternative to using such chemical pesticides is natural products such as essential oils in insecticidal action. Despite the fact of being effective, essential oils are unstable, poorly soluble in water, and degrade from the action of light, oxygen even at moderate temperatures. Thus, the nanostructuring of essential oils could circumvent such problems and ensure its effectiveness. The following study aimed to assess for the first time the effects of nanostructured systems of essential oils of Cymbopogon flexuosus, Eucalyptus globulus and Melaleuca alternifolia in subterranean termites (Coptotermes gestroi). The results showed that the solid lipid nanoparticles of M. alternifolia have both repellent and insecticide action. The following study showed that nanostructuring of essential oils with insecticidal action is a promising tool in the fight against termites.
Microbial ecology, Jan 21, 2017
It has been suggested that food storage inside the nest may offer termites with a nutritional pro... more It has been suggested that food storage inside the nest may offer termites with a nutritional provision during low resource availability. Additionally, feces employed as construction material provide an excellent environment for colonization by microorganisms and, together with the storage of plant material inside the nest, could thus provide some advantage to the termites in terms of lignocellulose decomposition. Here, we conducted for the first time a comprehensive study of the microbial communities associated to a termite exhibiting food storage behavior using Illumina sequencing of the 16S and (ITS2) regions of rRNA genes, together with enzymatic assays and data collected in the field. Cornitermes cumulans (Syntermitinae) stored grass litter in nodules made from feces and saliva located in the nest core. The amount of nodules increased with nest size and isolation, and interestingly, the soluble fraction of extracts from nodules showed a higher activity against hemicellulosic su...
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Papers by Ana Maria Costa Leonardo