Incipient Colonies Research Articles

Origin of termite eusociality: trophallaxis integrates the social, nutritional, and microbial environments

1. Numerous cladistic analyses have converged: termites are a monophyletic clade embedded within the paraphyletic cockroaches, and sister group to the biparental, wood‐feeding cockroach Cryptocercus. The latter is, therefore, an appropriate model for testing assumptions regarding early termite evolution.2. The ground plan of the termite ancestor is reviewed based on shared characters of ecology, life history, and behaviour in Cryptocercus and incipient termite colonies, and includes two levels of dependence: a reliance of all individuals on gut microbiota, and dependence of early instars on parental care. Both these conditions co‐evolved with parent‐to‐offspring proctodeal trophallaxis.3. The termite ancestor lived in a single log serving as food and nest. This ‘one‐piece’ nesting ecology prioritises nitrogen conservation and strongly influences interacting social, nutritional, and microbial environments. Each of these environments individually and in combination profoundly affect cockroach development.4. Proctodeal trophallaxis integrates the social, nutritional, and microbial environments. A change in trophallactic behaviour, from parental to alloparental, can, therefore, shift developmental trajectories, ultimately adding a third level of dependence. The death of gut protists during the host molting period and consequent interdependence of family members shifted the hierarchical level at which selection acted; fixation of eusociality quickly followed.5. The basic nesting ecology did not change when termites evolved eusociality, the change occurred in the allocation and use of existing resources within the social group, driven by nitrogen scarcity, mediated by trophallaxis, and made possible by a strongly lineage‐specific set of life history characteristics.

Hybridization of two major termite invaders as a consequence of human activity.

While hybridization of an invasive species with a native species is a common occurrence, hybridization between two invasive species is rare. Formosan subterranean termites (Coptotermes formosanus) and Asian subterranean termites (C. gestroi) are both ecologically successful and are the two most economically important termite pests in the world. Both species have spread throughout many areas of the world due to human activity; however, their distributions overlap in only three narrow areas because of distinct ecological requirements. In south Florida, where C. formosanus and C. gestroi are both invasive, the dispersal flight seasons of both species overlapped for the first time on record in 2013 and 2014. Pairings of heterospecific individuals were readily observed in the field and C. gestroi males preferentially engaged in mating behavior with C. formosanus females rather than females from their own species. In the laboratory, heterospecific and conspecific pairings had an equal colony establishment rate, but heterospecific incipient colonies had twice the growth rate of conspecific incipient colonies, suggesting a potential case of hybrid vigor. As all pre-zygotic barriers were lifted between the two species in the field, the apparent absence of post-zygotic barriers in the laboratory raises the possibility for introgressive hybridization in south Florida. While laboratory observations remain to be confirmed in the field, and the alate hybrid fertility is currently unknown, our results raise a tangible concern about the hybridization of two major destructive pest species. Such hybridization would likely be associated with a new economic impact.

Founding weaver ant queens (Oecophylla longinoda) increase production and nanitic worker size when adopting non-nestmate pupae.

Weaver ants (Oecophylla longinoda Latreille) are used commercially to control pest insects and for protein production. In this respect fast colony growth is desirable for managed colonies. Transplantation of non-nestmate pupae to incipient colonies has been shown to boost colony growth. Our objectives were to find the maximum number of pupae a founding queen can handle, and to measure the associated colony growth. Secondly, we tested if transplantation of pupae led to production of larger nanitic workers (defined as unusually small worker ants produced by founding queens in their first batch of offspring). Forty-five fertilized queens were divided into three treatments: 0 (control), 100 or 300 non-nestmate pupae transplanted to each colony. Pupae transplantation resulted in highly increased growth rates, as pupae were readily adopted by the queens and showed high proportions of surviving (mean = 76%). However, survival was significantly higher when 100 pupae were transplanted compared to transplantation of 300 pupae, indicating that queens were unable to handle 300 pupae adequately and that pupae require some amount of nursing. Nevertheless, within the 60-day experiment the transplantation of 300 pupae increased total colony size more than 10-fold whereas 100 pupae increased the size 5.6 fold, compared to control. This increase was due not only to the individuals added in the form of pupae but also to an increased per capita brood production by the resident queen, triggered by the adopted pupae. The size of hatching pupae produced by the resident queen also increased with the number of pupae transplanted, leading to larger nanitic workers in colonies adopting pupae. In conclusion, pupae transplantation may be used to produce larger colonies with larger worker ants and may thus reduce the time to produce weaver ant colonies for commercial purposes. This in turn may facilitate the implementation of the use of weaver ants.

Social structure varies with elevation in an Alpine ant.

Insect societies vary greatly in social organization, yet the relative roles of ecological and genetic factors in driving this variation remain poorly understood. Identifying how social structure varies along environmental gradients can provide insights into the ecological conditions favouring alternative social organizations. Here, we investigate how queen number variation is distributed along elevation gradients within a socially polymorphic ant, the Alpine silver ant Formica selysi. We sampled low- and high-elevation populations in multiple Alpine valleys. We show that populations belonging to different drainage basins are genetically differentiated. In contrast, there is little genetic divergence between low- and high-elevation populations within the same drainage basin. Thus, elevation gradients in each of the drainage basins represent independent contrasts. Whatever the elevation, all well-sampled populations are socially polymorphic, containing both monogynous (= one queen) and polygynous (=multiple queen) colonies. However, the proportion of monogynous colonies per population increases at higher elevation, while the effective number of queens in polygynous colonies decreases, and this pattern is replicated in each drainage basin. The increased prevalence of colonies with a single queen at high elevation is correlated with summer and winter average temperature, but not with precipitation. The colder, unpredictable and patchy environment encountered at higher elevations may favour larger queens with the ability to disperse and establish incipient monogynous colonies independently, while the stable and continuous habitat in the lowlands may favour large, fast-growing polygynous colonies. By highlighting differences in the environmental conditions favouring monogynous or polygynous colonies, this study sheds light on the ecological factors influencing the distribution and maintenance of social polymorphism.

Developmental instability in incipient colonies of social insects.

Social insect colonies can provide homeostatic conditions that buffer the incidence of environmental fluctuations on individuals, which have contributed to their ecological success. Coptotermes (Isoptera: Rhinotermitidae) is a highly invasive termite genus and several species have important economic impact in many areas of the world. Mature Coptotermes colonies with millions of individuals can provide optimal environmental condition and nurturing capacity for the developing brood. However, it was previously suggested that contrary to mature colonies, incipient colonies may be exposed to critical stress, which may explain for the low success rate of establishment within the first year of the life of a termite colony. We here investigated the stress imposed on individuals of incipient colonies by comparing the developmental instability of individuals between incipient and mature colonies of two Coptotermes species, C. formosanus Shiraki and C. gestroi (Wasmann). We assessed the developmental instability by measuring the asymmetry of morphological traits from the head capsule of the soldier caste. Soldiers from incipient colonies of both species displayed strong asymmetrical traits in comparison to soldiers from mature colonies. We suggest that homeostatic conditions for optimal development are reached as the colony matures, and confirmed that the incipient colony remains a critical bottleneck where individuals are exposed to high developmental stress.

The production of soldiers and the maintenance of caste proportions delay the growth of termite incipient colonies

In a termite colony, the incipient phase is the most critical part of the life of the colony. The quality of the investment in the first offspring by the primary reproduc- tives may determine the rate of success of the colony to survive the first year and its growth rate in the following years. However, termite colonies possess a physiological constraint, forcing the group to maintain a relatively fixed caste proportion. During the development of the incipient colony, there is therefore a conflict for the group on the developmental pathways of larvae into workers or soldiers. On the one hand, the more workers produced, the more work forces would be available to provide for the primary re- productives, the brood and the nest maintenance (overall nurturing capacity). On the other hand, some larvae must develop into soldiers to maintain the caste proportion, reducing the potential number of workers. Using incipient colonies of Coptotermes gestroi (Wasmann), we investi- gated the cost of maintaining the soldier proportion over the growth of the colony within the first year. Our results showed that an incipient colony maintains a stable soldier proportion regardless of the stress imposed. The resources redirected into the replacement of soldiers not only reduced the total number of workers, but it also reduced the overall growth of the colony by delaying the development of the remaining eggs. Our observations suggest that in termite incipient colonies, because of physiological constraints, the maintenance of the soldier proportion overrides the devel- opment of the colony.

Colony age-dependent pathway in caste development of Coptotermes formosanus Shiraki

The caste developmental pathway for the production of soldiers and nymphs in termite colonies is variable among species and limited numbers of studies have properly categorized such pathways. In this study, the developmental pathway for the production of soldiers and nymphs in Coptotermes formosanus Shiraki has been re-analyzed using the data from previous studies in light of new observations. Five distinct colony life stages were determined based on the caste developmental pathway used by the colony at each stage, which we here redefined as: incipient colony, immature colony, juvenile colony, mature colony, and senescent colony. We determined that in incipient colonies, the first soldier (nanitic) emerges from a second instar larva. We suggest that the production of a nanitic soldier is cost-effective as it allows the colony to focus on the production of workers from the first cohort of individuals. However, in an immature colony, the origin for the production of soldiers shifts to first and second instar workers. In juvenile colonies, soldiers are essentially produced from second instar workers. In mature colonies (>5 years), soldiers are mostly produced from second instar workers, occasionally from third instar workers, and we suggest that nymphs are primarily produced from second instar larvae. Finally, in senescent colonies, the absence of brood leads to the accumulation of old individuals. We concluded that descriptions from previous studies may have overlooked the group dynamics within a colony and that the caste developmental pathway in C. formosanus is dependent on the age of the colony.

Population Growth Characteristics of Incipient Colonies of the Eastern Subterranean Termite, Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae)

Growth of Reticulitermes flavipes (Kollar) incipient colonies during their first year was documented via a monthly destructive sampling census of 15 unique colonies, each headed by an inbred primary pair, for a total of 180 colonies. King and queen biomass greatly decreased during the first 2 months, coinciding with egg production and colony foundation, but their biomass remained relatively constant thereafter. Three cohorts of eggs were produced, with the greatest number of eggs (mean = 14.5) during the first month. Larvae were present at 1 month, and workers were first observed at 2 months. The survival rate of the initial brood was less than 100%, most likely due to cannibalism. A single soldier was first noted in some colonies at 6 months. Offspring biomass was equal to that of the reproductive pair at the 2-month census, double at 3 months, and quadruple at 11 months. One-year-old colonies ranged in size from 20 to 40 individuals, with an average of 28.9 individuals; total colony biomass was 39.8 mg. The growth rate of these R. flavipes colonies was much slower than was reported in other studies, but our observations are consistent with previous models and suggestions regarding colony growth.

Social influences on body size and developmental time in the bumblebee Bombus terrestris

In many social insects, including bumblebees, the division of labor between workers relates to body size, but little is known about the factors influencing larval development and final size. We confirmed and extend the evidence that in the bumblebee Bombus terrestris the adult bee body size is positively correlated with colony age. We next performed cross-fostering experiments in which eggs were switched between incipient (before worker emergence) and later stage colonies with workers. The introduced eggs developed into adults similar in size to their unrelated nestmates and not to their same-age full sisters developing in their mother colony. Detailed observations revealed that brood tending by the queen decreases, but does not cease, in young colonies with workers. We next showed that both worker number and the queen presence influenced the final size of the developing brood, but only the queen influence was mediated by shortening developmental time. In colonies separated by a queen excluder, brood developmental time was shorter in the queenright compartment. These findings suggest that differences in body size are regulated by the brood interactions with the queen and workers, and not by factors inside the eggs that could vary along with colony development. Finally, we developed a model showing that the typical increase in worker number and the decrease in brood contact with the queen can account for the typical increase in body size. Similar self-organized social regulation of brood development may contribute to the optimization of growth and reproduction in additional social insects.

Regional variation in queen and worker aggression in incipient colonies of the desert ant Messor pergandei

The fate of queen foundress associations in ants varies across taxa: in some, lethal fighting results in survival of a single queen, while in others, queens coexist long term. One hypothesis for this difference is that selection favors fighting when group sizes are small and tolerance when groups are large. In an experiment with the ant Messor pergandei, we formed small, medium, and large groups with newly mated queens from field populations that have different mean group sizes and differ in whether multiple queens occur in older established colonies. We found that whether queens are eliminated by fighting depends upon region of origin and not group size: regardless of co-foundress number, queens from sites with single-queen adult field colonies displayed agonistic behaviors and their colonies reduced to a single queen, while queens from sites with multiple-queen colonies did not fight and co-foundresses coexisted long term. Worker aggression towards and elimination of queens were also correlated with region of origin. Where fighting occurred, queens were as likely to be killed by workers as by other queens. An aggressive display was the most common form of agonistic interaction among queens, while fighting was relatively rare. We hypothesize that queen displays evolved in response to worker attacks because they increase the probability that workers will eliminate competitor queens. Our results suggest that the evolutionary interests of workers, as well as queens, could be important in determining the evolution and maintenance of queen elimination in foundress associations.

Reproductive restraint without policing in early stages of a social insect colony

Punishment of cheaters is a widespread means of promoting cooperation in social groups. In the eusocial Hymenoptera, punishment (i.e. ‘policing’) of reproductively active workers is thought to have been essential for the evolution of near-sterile worker castes. Many studies have investigated the evolutionary origin of policing behaviour in social insects, but few have considered the factors that affect the expression of policing behaviour in extant species. One factor that is predicted to affect the expression of policing behaviour is colony age. Specifically, policing is expected to be strongest at early stages of colony growth, when the cost of worker reproduction is high, and weaker at later stages. In a previous study, we found that egg-eating behaviour (i.e. ‘policing’, where workers eat worker-laid eggs) is not expressed in early stages of colony growth in the carpenter ant Camponotus floridanus , contrary to theoretical predictions. Here we test two other mechanisms of policing in incipient colonies: queen policing and destruction of male larvae. We found no evidence of either. We also found that workers from incipient colonies were capable of activating their ovaries and laying eggs. In the absence of evidence of policing in incipient C. floridanus colonies, we suggest that reproductive restraint by workers in early colony stages can arise because the inclusive fitness benefits of helping outweigh the direct benefits of reproducing. • It is argued that social insect worker castes required policing to evolve. • We found no evidence of policing in a carpenter ant in early colony development. • We also found no evidence that male larvae are eliminated at this colony stage. • Policing is not necessary to enforce worker sterility in some extant social insects.

Costs of pleometrosis in a polygamous termite

Costs and benefits of pleometrosis, as understood from social Hymenoptera, have never been tested in the independently evolved termites. To understand the extent to which such co-founding may be advantageous for colony survival and growth, we tracked the survival and reproduction of 5000 laboratory-established incipient colonies of the facultatively polygamous neotropical termite Nasutitermes corniger. Significantly more pleometrotic groups than monogamous queen-king pairs failed within the first 90 days of establishment, and 99 per cent of pleometrotic groups lost at least one founding member. Oviposition commenced earlier in larger groups, but colony growth was slower and production of workers and soldiers was delayed compared with pairs. Thus, pleometrosis does not increase colony fitness and is in fact highly disadvantageous.

Cellulolytic Protist Numbers Rise and Fall Dramatically in Termite Queens and Kings during Colony Foundation

Among the best-known examples of mutualistic symbioses is that between lower termites and the cellulolytic flagellate protists in their hindguts. Although the symbiosis in worker termites has attracted much attention, there have been only a few studies of protists in other castes. We have performed the first examination of protist population dynamics in queens and kings during termite colony foundation. Protist numbers, as well as measurements of hindgut and reproductive tissue sizes, were undertaken at five time points over 400 days in incipient colonies of Reticulitermes speratus, as well as in other castes of mature colonies of this species. We found that protist numbers increased dramatically in both queens and kings during the first 50 days of colony foundation but began to decrease by day 100, eventually disappearing by day 400. Hindgut width followed a pattern similar to that of protist numbers, while ovary and testis widths increased significantly only at day 400. Kings were found to contain higher numbers of protists than queens in incipient colonies, which may be linked to higher levels of nutrient transfer from kings to queens than vice versa, as is known in some other termite species. Protists were found to be abundant in soldiers from mature colonies but absent in neotenics. This probably reflects feeding of soldiers by workers via proctodeal trophallaxis and of reproductives via stomodeal trophallaxis. The results reveal the dynamic nature of protist numbers during colony foundation and highlight the trade-offs that exist between reproduction and parental care during this critical phase of the termite life cycle.

Towards a nutritional ecology of invasive establishment: aphid mutualists provide better fuel for incipient Argentine ant colonies than insect prey

Many potential species invasions fail before establishment. This is likely especially true for invasive Argentine ants that must overcome a severe founding bottleneck and transition from propagules that rely on protein-rich prey to massive supercolonies that dominate by consuming carbohydrate-rich honeydew from hemipteran mutualists. While this dietary shift supports the classic idea that protein fuels early colony development and carbohydrates maintain adult workers, recent evidence suggests that carbohydrates can govern initial colony establishment. In this study, we use lab experiments to show that resources from aphid mutualists had greater benefits for Argentine ant propagule survival, maintenance, growth, and worker activity rates than did prey items. These effects persisted at low aphid densities, and when colonies were otherwise starved. Moreover, prey-starved colonies did not appear to consume aphids, suggesting that carbohydrate-rich honeydew is a mechanism that facilitates colony establishment. Combined, these results support a hypothesis that the dietary shift from prey to honeydew is driven more by increased access to hemipterans after establishment, than by specific benefits of prey early in colony development. The results highlight the important role of nutritional ecology for studying invasive establishment, linking propagule success not only to the supply of food resources, but also to their quality.

Termite Soldier Differentiation in Incipient Colonies is Related to Parental Proctodeal Trophallactic Behavior

Termite soldiers represent a peculiar caste among social insects in terms of their specific defensive roles. Numbers of soldiers are relatively low in a mature colony, and it is impossible to identify the individuals that will differentiate into soldiers. If it were possible to specify these individuals prior to soldier differentiation, it would facilitate a better understanding of the regulatory mechanisms of soldier differentiation under natural condition. Here we analyzed soldier differentiation in incipient colonies of Zootermopsis nevadensis, in which only a single soldier develops via a presoldier stage, and is stable during early colony ontogeny. We observed that the oldest third instar differentiated into a presoldier within about eight days from its appearance. Caste differentiation, however, was not strictly determined on an individual basis. The oldest third instars never differentiated into presoldiers if primary reproductives were removed soon after their appearance. Behavioral observations of primary reproductives and their offspring prior to presoldier differentiation, showed that primary reproductives transferred proctodeal materials to the oldest third instar significantly more frequently than to other larva. A high juvenile hormone (JH) titer is required for the soldier differentiation, and we suggest that the JH itself or some nutrients/factors increasing larval JH titer may be transferred to the oldest third instar via a parental proctodeal fluid.

Fusion between Southeastern United States Argentine Ant Colonies and Its Effect on Colony Size and Productivity

Abstract The ecological success of invasive ants has been linked to their ability to form expansive supercolonies. In the Argentine ant, Linepithema humile (Mayr), increased productivity and competitive ability of introduced supercolonies in several places, e.g., California and southern Europe, has been linked to high population densities that could have been attained via fusion of nonaggressive and genetically similar nests. Recently, we have found that introduced L. humile colonies in the southeastern United States, which have higher levels of intraspecific aggression and genetic diversity than those in California and southern Europe, sometimes also fuse; yet it is unclear what the longer term consequences of such colony fusion might be. In this study, we examined whether fusion of these southeastern United States L. humile colonies results in larger colonies by recording colony size and productivity in pairs that fused and in pairs that did not fuse. After 6 mo, colonies that fused produced 47% more workers and had twice as many queens as colony pairs that did not fuse. Also, fused colonies had an overall per capita colony productivity (number of brood and workers produced per queen and per worker) comparable to that of nonfused pairs and unpaired controls. Furthermore, all queens contributed to worker pupae production in fused colonies. Thus, fusion of initially aggressive southeastern United States L. humile colonies results in colonies with higher worker number without decreasing per capita productivity. Moreover, offspring contribution by all queens in fused colonies may alter colony genotypic composition resulting in reduced intraspecific aggression that in turn promotes further fusion. This process may be relevant to the establishment of incipient colonies in areas where multiple introductions have occurred.

Development rate and brood production in haplo- and pleometrotic colonies of Oecophylla smaragdina

Pleometrosis (colony founding by multiple queens) may improve life history characteristics that are important for early colony survival. When queens unite their initial brood, the number of workers present when incipient colonies open may be higher than for single queen colonies. Further, the time until the first worker emerges may shorten. For territorial species and species that rob brood from neighbouring colonies, a faster production of more workers may improve the chance of surviving intraspecific competition. In this study, the time from the nuptial flight to the emergence of the first worker in incipient Oecophylla smaragdina Fabr. colonies founded by 1–5 queens was compared and the production of brood during the first 68 days after the nuptial flight was assessed. Compared to haplometrotic colonies, pleometrotic colonies produced 3.2 times more workers, their first worker emerged on average 4.3 days (8%) earlier and the queen’s per capita egg production almost doubled. Further, colony production was positively, correlated with the number of founding queens and time to worker emergence was negatively correlated. These results indicate that pleometrotic O. smaragdina colo-nies are competitively superior to haplometrotic colonies as they produce more workers faster and shorten the claustral phase, leading to increased queen fecundity.

Dispersal flight and colony development in the fungus-growing termites Pseudacanthotermes spiniger and P. militaris

Pseudacanthotermes spiniger and P. militaris are two African fungus-growing termites (Termitidae, Macrotermitinae) which may become pests in disturbed agrosystems where they often live in sympatry. To study their development and their reproductive strategies, colonies of both species were reared in the laboratory for 20 and 17 years, respectively, after their foundation from reproductive pairs. The first steps of development were in great part similar in both species, although P. spiniger favoured the defence during the juvenile period, while P. militaris tended to favour a rapid development. While P. spiniger colonies did not produce alates until year 7 of colony life, P. militaris colonies were able to produce a fertile progeny 4 years after their foundation. In contrast, major soldiers were more rapidly differentiated in the incipient colonies of P. spiniger. Dispersal flights occurred every year for 10 years in P. spiniger. In P. militaris, dispersal flights did not occur regularly although alates appeared yearly. The annual number of alates produced by P. spiniger increased with the colony age to reach a maximum of 25,000 individuals and global production of alates was estimated at ca. 150,000 individuals in the life of a colony. The longevity of P. spiniger and P. militaris colonies was around 20 years. These species were shown to be reproductively isolated by multiple pre-mating mechanisms. While chronological differences in dispersal flights contribute to reproductive isolation of the two species, the non-viability of experimental hybrid colonies also indicates the involvement of post-mating mechanisms of isolation.

The Effect of Queen and Worker Adoption on Weaver Ant (Oecophylla smaragdina F.) Queen Fecundity

Incipient ant colonies are often under fierce competition, making fast growth crucial for survival. To increase production, colonies can adopt multiple queens (pleometrosis), fuse with other colonies or rob brood from neighboring colonies. However, different adoption strategies might have different impacts such as future queen fecundity or future colony size. O. smaragdina queen production was measured in incipient colonies with 2, 3 or 4 founding queens, following the transplantation of 0, 30 or 60 pupae from a donor colony. Pupae developed into mature workers, resulting in increased worker/queen ratios in pupae transplanted treatments and leading to increases in the per capita queen production. Conversely, more queens did not induce increased per capita fecundity. Thus, brood robbing added individuals to the worker force and increased future production of resident queens, whereas queen adoption increased the colony’s future production, but not the production of individual queens.

Leaf endophyte load influences fungal garden development in leaf-cutting ants

BackgroundPrevious work has shown that leaf-cutting ants prefer to cut leaf material with relatively low fungal endophyte content. This preference suggests that fungal endophytes exact a cost on the ants or on the development of their colonies. We hypothesized that endophytes may play a role in their host plants’ defense against leaf-cutting ants. To measure the long-term cost to the ant colony of fungal endophytes in their forage material, we conducted a 20-week laboratory experiment to measure fungal garden development for colonies that foraged on leaves with low or high endophyte content.ResultsColony mass and the fungal garden dry mass did not differ significantly between the low and high endophyte feeding treatments. There was, however, a marginally significant trend toward greater mass of fungal garden per ant worker in the low relative to the high endophyte treatment. This trend was driven by differences in the fungal garden mass per worker from the earliest samples, when leaf-cutting ants had been foraging on low or high endophyte leaf material for only 2 weeks. At two weeks of foraging, the mean fungal garden mass per worker was 77% greater for colonies foraging on leaves with low relative to high endophyte loads.ConclusionsOur data suggest that the cost of endophyte presence in ant forage material may be greatest to fungal colony development in its earliest stages, when there are few workers available to forage and to clean leaf material. This coincides with a period of high mortality for incipient colonies in the field. We discuss how the endophyte-leaf-cutter ant interaction may parallel constitutive defenses in plants, whereby endophytes reduce the rate of colony development when its risk of mortality is greatest.