Polygyny in the Neotropical termite Nasutitermes corniger: life history consequences of queen mutualism

Summary ecological aspects of monogyny and polygyny in social insect colonies are important in comparing individual queen reproductive success. Inseminated, fecund, multiple foundresses are common in some groups of ants and eusocial wasps, but true polygyny in termites has not previously been studied. One third of Nasutitermes corniger (Isoptera: Termitidae) colonies sampled in areas of young second growth in Panama contained from 2–33 primary queens (not supplementary or neotenic reproductives). All queens in polygynous associations were fully pigmented, physogastric egg layers within a single royal cell. Multiple kings were found less frequently; true polyandry is apparently restricted to immature polygynous colonies.Data on queen weight and morphological features, and on colony composition, show that queens in polygynous nests are young and that a transition from polygyny to monogyny probably occurs after several years. The escalated growth rate of multiple queen colonies removes them from the vulnerable incipient colony size class more rapidly than colonies initiated by a single foundress, and gives them sufficient neuter support staff (workers and soldiers) to enable earlier production of fertile alates. Using a population model (Leslie matrix) I construct isoclines of equal population growth which show values of early age class probability of survival and reproductive output favoring monogyny or polygyny under individual selection. This model of queen mutualism accounts for the risk of a female in a polygynous group not succeeding as the final surviving queen.Multiple primary queens are considered rare in termites, but a review of the literature demonstrates that they may be more widespread than is currently recognized. Polygyny in termites has received scant attention but is of significance as an example of a further ecological and evolutionary convergence between the phylogenetically independent orders Isoptera and Hymenoptera.     

Defensive behavior of the black widow spider Latrodectus hesperus (Araneae: Theridiidae)

Summary When threatened, the black widow spider, Latrodectus hesperus, emits an adhesive, viscous web, pulls the strand from its spinnerets with its fourth pair of legs, and spreads its appendages. This behavior positions the web over the delicate abdomen, increases the area of protection, and enables the spider to place the web onto the offender, if necessary.In laboratory interactions, the viscous web protected black widows from mice (Peromyscus spp.). Mature female spiders, which had their spinnerets blocked and hence could not discharge the viscid silk, escaped less often than did black widows that were not experimentally altered.The viscid silk is palatable to mice and it appears that the deterrent effect of the web is due solely to mechanical irritation.The defensive behavior is elicited most often from mature females, which may suffer greater predation than other age groups. Males lose the ability to produce the defensive web at maturity and may shift their energy resources totally into reproductive effort.     

Replacement of reproductives in Nasutitermes princeps (Desneux) (Isoptera: Termitidae)

Summary The production of replacement reproductives in experimentally orphaned societies was investigated in Nasutitermes princeps (Desneux). From 1 to 180 replacement queens and multiple kings, all adultoids, were found in the 13 nests that were re-collected. Normal imagos, microimagos, or a mixture of the two forms were present, depending on colony composition at the time of orphaning. In colonies with alates, the corresponding forms were found as replacement reproductives. Where only young nymphs were present, microimagos differentiated. Neither the number of queens nor their level of physogastry was correlated with the time elapsed since orphaning, but the total egg-laying rates were. We suggest that competition among queens rather than time determines individual physogastric development. Observations show that the most likely cause of accidental queen death in nature is probably nest fall from the supporting tree. Even in this case, the queen may be able to migrate to a newly rebuilt nest. An experimental simulation of this situation showed that colony migration can occur. The data indicate that the replacement of the primary queen after her accidental death cannot by itself account for the high rate of polygyny (60%) encountered in N. princeps. Two other possible causes are the replacement of the ageing foundress as a normal event of colony life, and colony reproduction by budding off new nests with adultoid reproductives.King Léopold III Biological Station, Laing Island, Papua New Guinea, contribution no. 84Research Assistant of the National Fund for Scientific Research (Belgium)     

Defensive behavior of ants in a mutualistic relationship with aphids

Mutualistic relationships between ants and aphids are well studied but it is unknown if aphid-attending ants place a greater relative importance on defending aphids from aphid-predators or from competing ant colonies. We tested the hypothesis that aphid-attending ants defend their aphids against aphid-predators more aggressively than against ants from neighboring colonies. We conducted introduction trials by placing an individual non-predatory insect, an aphid-predator, or a foreign conspecific ant on the leaf of a resident ant. We found that ants did not attack non-predatory insects, but did attack competing ants and aphid-predators. When we presented resident ants with both the threats (i.e., predator and competitor) at the same time, residents always attacked potential competitors as opposed to aphid-predators. We suggest this behavior may reduce the likelihood of raids by neighboring colonies. Ants appear to balance both the energetic costs of making an attack and the costs associated with losing aphids to a predator, against the benefits of signaling their defensive ability to rivals and/or preventing rivals from gaining knowledge of a potential food resource.     

Defensive secretions from the larvae ofApatania fimbriata (Pictet) (Trichoptera: Limnephilidae)

Summary When the larvae of the caddis flyApatania fimbriata (Pictet) are threatened, drops of fluid appear on their head capsules. The secretions are produced in a gland in the dorsal part of the prothorax. The neck region contains an eversible sac with numerous single setae, groups of 3 setae, or rows of setae on the surface. The secretion is released through two paris of orifices on the lateral sides of the sac. For the most part the secretion is composed of some 30 fatty acids, with the major components having 12–14 carbon atoms and up to 4 double bonds (approx. 1–2 µg secretion per specimen). Biotests with synthetic saturated acids (C₆–C₁₂) in a stream and in the laboratory demonstrated a paralysing effect on small invertebrate predators (Rhyacophila sp.,Plectrocnemia conspersa, Hydropsyche sp., larvae, all Trichoptera). In choice experiments,Rhyacophila sp. larvae preferred larvae ofAgapetus fuscipes andDrusus annulatus (Trichoptera) as food as compared withApatania fimbriata larvae. Larger predators, such asDinocras cephalotes (Insecta, Plecoptera) and the fishCottus gobio, did not discriminate betweenApatania fimbriata and other prey species. The use of fatty acids in defensive secretions is interpreted as an adaptation to the running water environment. They are effective repellents againstRhyacophila sp. larvae, the most important predator in the natural environment ofApatania larvae.     

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

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. Received: 18 March 1998 / Accepted after revision: 31 May 1998     

Relatedness,recognition errors,and colony fusion in the termite <Emphasis Type="Italic">Nasutitermes corniger</Emphasis>

Loss of aggression between social groups can have far-reaching effects on the structure of societies and populations. We tested whether variation in the genetic structure of colonies of the termite Nasutitermes corniger affects the probability of aggression toward non-nestmates and the ability of unrelated colonies to fuse. We determined the genotypes of workers and soldiers from 120 colonies at seven polymorphic microsatellite loci. Twenty-seven colonies contained offspring of multiple founding queens or kings, yielding an average within-colony relatedness of 0.33. Genotypes in the remaining 93 colonies were consistent with reproduction by a single queen and king or their progeny, with an average within-colony relatedness of 0.51. In standardized assays, the probability of aggression between workers and soldiers from different colonies was an increasing function of within-colony relatedness. The probability of aggression was not affected significantly by the degree of relatedness between colonies, which was near zero in all cases, or by whether the colonies were neighbors. To test whether these assays of aggression predict the potential for colony fusion in the field, we transplanted selected nests to new locations. Workers and soldiers from colonies that were mutually tolerant in laboratory assays joined their nests without fighting, but workers and soldiers that were mutually aggressive in the assays initiated massive battles. These results suggest that the presence of multiple unrelated queens or kings promotes recognition errors, which can lead to the formation of more complex colony structures.     

The organisation of collective foraging in the harvester termite Hodotermes mossambicus (Isoptera)

Summary The process by which the foragers build up a foraging system between the nest hole and the food source, starting from an initial random distribution, was investigated under conditions of both light and dark in the laboratory.The extent to which trail pheromone is used can be determined by observing the abdominal position of workers moving outside the nest and can be classified into three categories, namely no trail-laying, marking and directional trail-laying.When workers of this species emerge from the nest hole into light emitted from a certain direction they orientate photo-menotactically. First, they mark the area around the nest hole, moving in small loops; they then make larger exploratory loops without trail-laying. Once they find a source of food they return directly to the immediate vicinity of the nest hole. As the area around the hole has already been marked it is easy for the termites to locate the hole. When a piece of food has been deposited by the hole the termites display directional trail-laying behaviour by leaving a trail in the direction of the source of food, this trail being stronger nearer the nest and decreasing as it approaches its goal. Inexperienced explorers are biased in this direction with a statistically higher frequency. If successful they join in the foraging and repeatedly contribute to the trail, which then gradually brings together most of the foraging population.In darkness exploratory loops are made with continuous marking, always returning to the nest hole, whereby a scent gradient decreasing away from the hole is formed. Once a source of food has been discovered the termites are neither able to return directly to the nest hole nor to return along their outward marking trail. They leave marking trails making exploratory loops from the food source with successively increasing radii. Another scent gradient, decreasing outwards from the food, is created. If the termite reaches the increasing scent around the nest hole from the decreasing scent around the food source it will locate the hole chemotactically. As other food finders repeatedly cross from one field to the other the scents will combine and become concentrated, thus forming a foraging path.     

Lack of evidence for nepotism by workers tending queens of the polygynous termite <Emphasis Type="Italic">Nasutitermes corniger</Emphasis>

Kin selection theory predicts that workers in social insect colonies should preferentially aid close relatives over less related or unrelated individuals if such behaviors increase inclusive fitness. For example, a worker in a polygynous (multiple-queen) colony is predicted to tend its own mother rather than an unrelated queen if this nepotistic behavior increases its mother’s reproductive success in excess of costs. Despite predictions, experimental tests conducted in the social Hymenoptera have found no clear evidence of nepotism. No tests for nepotism have been carried out in the Isoptera (termites), another major insect taxon showing highly developed sociality. We tested for nepotistic behavior in the termite Nasutitermes corniger by determining if workers preferentially fed and groomed their mothers in a laboratory assay. We collected workers from nine naturally occurring multiple-queen colonies as they tended queens and determined their parentage using highly variable microsatellite markers. Our results provide no evidence that workers tend their mothers in preference to co-occurring queens. The absence of evidence for nepotism is consistent with previous results reported from numerous studies of eusocial hymenopterans.     

Dynamics of biparental care in the dampwood termite,Zootermopsis nevadensis (Hagen): response to nitrogen availability

Summary Studies were conducted on the dampwood termite, Zootermopsis nevadensis, to examine the behavioral roles of the reproductive pair during the nest-founding period and to determine the effect of nitrogen availability on their reproduction and division of labor. Nitrogen has been hypothesized to be an important limiting nutrient for founding pairs. One nitrogenous reserve, uric acid-nitrogen, was examined in reproductives and in nutrient-receiving and nutrient-gathering colony members; it was found in highest amounts in the reproductives (i.e., alates, de-alates, and primary reproductives). Young pairs may use these nitrogenous reserves to increase their chances for reproduction. In support of this hypothesis, founding pairs that were fed a diet supplemented with uric acid-nitrogen had a significantly greater probability of producing at least one offspring than did pairs fed an unsupplemented diet. Females that were fed a nitrogen-poor diet restricted their total activity while their mates sustained a high activity during colony initiation. When fed a nitrogen-rich diet, females collected pulp more often than their mates, while males collected more water, though only in the period prior to egg laying. In all pairs, males transferred proctodeal pellets (food derived from the hindgut intestine) to their mates significantly more often than females to males, and females fed on proctodeal pellets significantly more often than did their mates. The male-female asymmetries in pellet transfer and feeding were not significant in the stage after egg deposition. Once eggs and larvae were present in the nest, a male and female spend an equal percentage of time caring for eggs and feeding larvae. Proctodeal pellets examined in reproductives were found to be rich in proteins. This suggests that in the pre-egg period, the male provides nitrogen-rich substances to the female as a form of paternal investment.     

Diving behavior of immature hawksbills (Eretmochelys imbricata) in a Caribbean cliff-wall habitat

Time-depth recorders were attached to immature hawksbills (Eretmochelys imbricata Linnaeus, 1766) residing at the northwestern cliffs of Mona Island, Puerto Rico. Data on diving profiles obtained from four turtles of 32.0 to 53.4 cm straight carapace length revealed strong similarities in behavioral patterns. During daylight hours, turtles were active an average 8.4 h per day, surfacing 3.6% of the time. Length of foraging dives correlated with turtle size, with mean durations ranging from 8.6 to 14.0 min. Foraging dives, with a mean depth of 4.7 m, were associated with feeding on encrusting sponges. At night, turtles were mostly inactive, surfacing 1.8% of the time and with individual mean submergence intervals of between 30.4 and 37.1 min. From the surfacing behavior of turtles making deep and long dives, it is inferred that dives were aerobic, with the turtles making use of oxygen stores in addition to that of the lung.     

Predatory behavior of Polybia sericea (Olivier), a tropical social wasp (Hymenoptera: Vespidae)

Summary Polybia sericea (Olivier) (Hymenoptera: Vespidae) foragers were trained to visit experimental foraging plots and tests were conducted to determine the role of visual, olfactory, and chemotactile cues in prey location. Foragers approached prey from downwind and hovered downwind of visual and olfactory stimuli. Olfactory cues were more likely to elicit landing than were visual cues. Biting of potential prey was most consistently elicited by a combination of visual, tactile, and chemotactile cues. Foragers encountering large prey carried a piece back to the nest and returned for prey remains. These returning foragers used visual cues to direct intensive aerial search; olfactory prey cues elicited landing.     

Homing behavior of wood thrushes (Hylocichla mustelina)

Summary Using the wood thrush (Hylocichla mustelina) as an example of a typical nocturnal migrant, we employed radio telemetry to follow breeding birds during the course of homing movements following displacements. Seven thrushes were displaced over distances of 6.5 to 17.3 km in a variety of directions from their nesting territories. The thrushes moved in a series of short flights (mean = 2.1 km) performed primarily at dawn. Consequently, the birds took several days to home from even these relatively short displacements. Thrushes flew under clear and solid overcast skies and even in light rain. The pooled individual flights of the birds were significantly oriented in the homeward direction (Fig. 2). Their orientation relative to home did not improve significantly as they progressed toward the goal. Three of the birds were documented to have returned to their home territories. The detailed tracks of the birds preclude the possibility that they homed by random search.     

Provisioning behavior and the estimation of investment ratios in a solitary bee,Calliopsis (Hypomacrotera) persimilis (Cockerell) (Hymenoptera: Andrenidae)

Summary One aspect of behavioral ecology that has received considerable attention, especially by students of social insects, is the relative amount of energy invested by parents in the rearing of male versus female offspring. Sexual selection theory makes predictions about how individuals should allocate their total investment in the sexes. To test these predictions we must accurately quantify the relative cost incurred by a parent in the production of an average individual of either sex. Body weight ratios are the most common estimate of cost ratio, but the correspondence between offspring body weight and energetic investment on the part of the parent has rarely been determined. Calliopsis (Hypomacrotera) persimilis is a solitary, ground-nesting bee whose natural history makes it particularly convenient for studies of investment patterns and foraging behavior. Each day females construct and provision from 1 to 6 cells in linear, closely-spaced series. Each cell is provisioned with pollen from Physalis Wrightii flowers, which is collected on two or three foraging trips. However, the temporal sequence in which two- and three-trip foraging bouts occur is not random. Females invariably begin each day provisioning cells with three trips worth of pollen and usually switch to provisioning the latter cells of the day with just two trips worth of pollen. The sex of the offspring within the same co-linear series of cells also varies non-randomly — female offspring predominate in the first cells of each series and male offspring in the latter cells. The correspondence between the number of foraging trips to provision a cell, the total time spent foraging, and offspring sex was determined for 36 cells. The data indicate a close, though not absolute, relationship between the number of foraging trips and the sex of the offspring: males usually received two trips of pollen, though some received three, whereas female offspring invariably received three trips worth of pollen. A number of potential estimates of the relative cost of female and male offspring production were calculated. Estimates of the cost ratio based on the amount of time spent foraging, adult dry body weight, and pollen ball dry weight all give similar values. Female offspring receive an energetic investment of from 1.3 to 1.5 times that of males. These results support the use of adult dry body weight ratios in the estimation of cost ratios.     

Chemical basis of nestmate recognition in a defense context in a one-piece nesting termite

Nestmate recognition is a necessary capacity for the occurrence of discrimination between nestmate and non-nestmate individuals. In one-piece nesting termites, which nest and forage in a single piece of wood, nestmate recognition is poorly studied mainly because the probability of encountering exogenous individuals is low in comparison with separate-piece nesting termites. Previous work described that production of soldiers of Neotermes chilensis, a one-piece nesting termite, increased when the risk of invasion of their colony increased, for example when neighboring colonies were present in the same nesting substrate and members of different colonies met when digging galleries. If soldiers are to fulfill their defensive role under these circumstances, they should show nestmate recognition ability; moreover, based on work on other social insects, such nestmate recognition should be based on cuticular compounds (CC). Bioassays were performed in which a soldier of N. chilensis was confronted with a nestmate or non-nestmate primary reproductive, pseudergate or another soldier, and in which a soldier was confronted with untreated and with CC-deprived dead primary reproductives. The results showed that soldiers were indeed more aggressive toward non-nestmates than nestmates for all castes, and that this discrimination was mediated mainly by qualitative (simple matching coefficient) and quantitative (Renkonen index) differences in CC.     

Mating behavior of Labidocera aestiva (Copepoda: Calanoida)

The calanoid copepod Labidocera aestiva Wheeler exhibits a ritualized mating behavior. Sensory hairs and spines and integumental pores on the male and female are believed to play a regulatory role in the mating encounter. Scanning electron microscopy (SEM) revealed approximately 20 unusual pore structures (pit-pores) on the right ventrolateral surface of the female's abdominal segment, the area where the spermatophore coupling device is attached. Prior to spermatophore transfer, the male vigorously strokes this area with the modified endopod of his left fifth leg to prepare the pit-pore region for attachment of a new spermatophore. Transmission electron microscopy (TEM) indicated that the cells underlying each pit-pore may have a secretory function. We hypothesize that the pit-pores secrete a substance which dissolves the cement binding the coupling device to the abdomen and aids the female to remove a discharged spermatophore from her urosome.Contribution No. 116, Harbor Branch Foundation, Inc.     

Mating behavior of Centropages typicus (Copepoda: Calanoida)

Observations were made on approximately 300 mating couples of Centropages typicus Krøyer. Mating behavior consists of 4 distinct stages: pre-copulation, spermatophore extrusion, copulation, and post-copulation. Successful copulation requires proper positioning of the spermatophore complex on the female urosome and is dependent upon precise movements and orientation of the male during the mating encounter. Sub-optimal mating encounters, resulting in the improper placement of the spermatophore complex, were observed and adaptations tending to reduce spermatophore wastage are discussed.Contribution No. 62, Harbor Branch Foundation, Inc.