The effect of stolon fragmentation on the colonization of clonal invasive Carpobrotus edulis in a coastal dune system: a field test

Disturbances usually initiate processes of fragmentation in clonal plants, with the consequent division into portions of different size. The ability of these portions to survive and regrow after fragmentation plays an important role in the maintenance of populations and the colonization of new environments. In this field experiment we aim to determine the importance of stolons as reserve organs in the colonization of a coastal sand dune by a clonal invader. We simulated an event of fragmentation of clones of an aggressive invader into portions with short and long stolon sizes. Our results showed a reduction of biomass allocation to roots in the long stolon treatment that was balanced by an increase in the above‐ground growth; consequently, the area colonized by the invader was greater. We report evidence that stolons can contribute to buffering stressful conditions and allow expansion of the invader into a natural coastal sand dune.     

Phenotypic plasticity of invasive Carpobrotus edulis modulates tolerance against herbivores

The anthropogenic movement of species has favoured the introduction of invasive plants worldwide. Invasive plants are frequently released from their natural enemies; however, new associations with generalist herbivores may induce defence mechanisms of non-native plants. Defensive traits are often directly related to the highly competitive ability, but also to potential antagonisms and mutualisms that they can establish with soil microorganisms. Here, we examined whether the intraspecific competition and soil microorganisms influence the morphological and physiological traits of Carpobrotus edulis when is being attacked by the native generalist snail Theba pisana. To achieve this, we grew two C. edulis individuals in separate and same pots filled with live or sterile sand, and with or without T. pisana. Our results indicated that herbivory induced an increase of shoot biomass in attacked C. edulis individuals (i.e., treated donor plants), as well as in un-attacked neighbouring individuals co-growing in the same pot (i.e., untreated recipient plants). Nevertheless, intraspecific competition nor soil microorganisms did not affect the growth of C. edulis despite reduced physiological activity and damage caused by the herbivore. Overall, our findings revealed that C. edulis individuals tolerate snail attack by inducing a compensatory growth response. We conclude that phenotypic plasticity of invasive C. edulis favours tolerance against herbivores, but we also suggest that plant-plant interactions probably determine the plant growth of un-attacked neighbouring C. edulis individuals, thus favouring their invasion mechanisms.

     

Physiological integration increases the survival and growth of the clonal invader <Emphasis Type="Italic">Carpobrotus edulis</Emphasis>

Clonal growth seems to be a common trait for many of the most aggressive invasive plant species. However, little research has been conducted to determine the role of clonality in the successful invasion of new areas by exotic species. Carpobrotus edulis (L.) N.E. Br. is a mat-forming succulent plant, native to South Africa that is invasive in coastal dunes of Australia, New Zealand, USA and Southern Europe. Although Carpobrotus edulis is a clonal plant, there is no information on the role of clonality for the invasion by this species, therefore the objective of this study was to test whether or not physiological integration improves the performance of C. edulis invading coastal sand dunes. To do that, a 6-month field experiment was designed in which the stolon connections between the apical ramets and the C. edulis mats were severed to prevent physiological integration. This treatment was applied to ramets growing under high and low competition with the native species. Apical ramets with intact stolon connections were used as control. Integration improved the survivorship and growth of apical ramets, both in high and low competition. Connected ramets showed a more pronounced increase of clonal growth (estimated as stolon length) during the experimental period and a higher total biomass and number of ramets at the completion of the experiment. In terms of survivorship, the benefit of integration was greater under high competition. Physiological integration can therefore be considered an important factor in the invasiveness of C. edulis, both in open space and in direct competition with the native plants.     

Assessing the residual effects of Carpobrotus edulis invasion, implications for restoration

We examined whether the residual effects on soil caused by the invasion of Carpobrotus edulis, common iceplant, would inhibit the reestablishment of a native plant species. Carpobrotus edulis interacts both directly by suppressing the growth and establishment of other plants and indirectly by altering soil chemistry. We tested whether the residual effects of C. edulis resulted in lowered germination, survival, growth, and reproduction of Gilia millefoliata, a rare dune annual. We compared G. millefoliata planted in plots previously occupied by C. edulis to G. millefoliata planted in plots that previously had native vegetation. Each plot received three treatments: seed, transplant, and unplanted, and were censused every three weeks until senescence. Carpobrotus edulis had strong negative effects on the germination, survival, growth, and reproduction of G. millefoliata. C. edulis lowers soil pH and increases organic content due to the recalcitrance of tissue to decomposition, which may have evolved as a mechanism to facilitate recolonization and invasion.     

Two types of division of labour in clonal plants: benefits, costs and constraints

Clonal plants spread vegetatively within their habitats by forming rooted ramets on stolons or rhizomes. Each of these ramets is capable of an independent existence after establishment. Nevertheless, ramets remain physically connected by stolon or rhizome internodes for variable periods of time, thereby allowing for resource movement and signal transduction within clones.Interconnected ramets of clonal plants, though potentially independent and totipotent, can specialize functionally in the performance of limited numbers of tasks such as the uptake of resources from above- vs below-ground sources, carbohydrate storage, vegetative spread and sexual reproduction. Such specialization and cooperation is comparable to a division of labour in economic systems or in colonies of social animals. The ecological significance of division of labour in clonal plants may be found in the increased efficiency of entire clones in exploiting their environments.Two different types of division of labour in clonal plants will be discussed in this review. The first type is an environmentally-induced specialization of ramets in the uptake of locally abundant resources (plastic division of labour), which can be found in several stoloniferous species. Evidence exists that this response increases resource uptake in spatially heterogeneous environments. The second type of division of labour, which occurs mainly in rhizomatous species, relates to a developmentally-programmed specialization and cooperation between interconnected ramets. This response pattern is thought to enhance plant performance by restricting the number of tasks for individual ramets and thereby significantly increasing the efficiency of task performance. In some plants, such an inherent division of labour is likely to contribute to nutrient extraction from poor and unpredictably variable sources.In this article not only benefits but also potential costs and constraints on division of labour in clonal plants are shown. The aim is to provide a review of existing knowledge and to develop concepts and hypotheses for future research.     

The evolutionary history of division of labour

Functional specialization, or division of labour (DOL), of parts within organisms and colonies is common in most multi-cellular, colonial and social organisms, but it is far from ubiquitous. Several mechanisms have been proposed to explain the evolutionary origins of DOL; the basic feature common to all of them is that functional differences can arise easily. These mechanisms cannot explain the many groups of colonial and social animals that exhibit no DOL despite up to 500 million years of evolution. Here, I propose a new hypothesis, based on a multi-level selection theory, which predicts that a reproductive DOL is required to evolve prior to subsequent functional specialization. I test this hypothesis using a dataset consisting of the type of DOL for living and extinct colonial and social animals. The frequency distribution of DOL and the sequence of its acquisition confirm that reproductive specialization evolves prior to functional specialization. A corollary of this hypothesis is observed in colonial, social and also within multi-cellular organisms; those species without a reproductive DOL have a smaller range of internal variation, in terms of the number of polymorphs or cell types, than species with a reproductive DOL.     

Spatial division of labour of Schoenoplectus americanus

If connected ramets are growing in heterogeneous environments, Division of Labour (DoL) among ramets potentially will result in more efficient sharing of resources and an overall benefit to the plants. As a result of DoL, connected ramets growing in a heterogeneous environment might achieve more biomass than ramets growing in a homogeneous environment. DoL has been demonstrated to occur in a few clonal plant species, although most studies simply focussed on biomass allocation, not on actual resource capturing such as water and nutrient consumption. The model system for our study is one in which two connected ramet groups of Schoenoplectus americanus were placed into contrasting environments. In one treatment, the connected ramets grew in heterogeneous environments and in the other treatment, the connected ramets grew in the same (i.e. homogeneous) environment. We manipulated two variables (light and salinity) in the experiment. We hypothesized that ramets growing in a shaded and fresh water condition in a heterogeneous environment would use more water than ramets growing in a similar condition but in a homogeneous environment. We further hypothesized that ramets growing in a light and saline condition in a heterogeneous environment would assimilate less water than ramets growing in a similar condition but in a homogeneous environment. These hypotheses are based on the assumption that ramets in a heterogeneous environment would translocate water from ramets growing in a shaded and fresh water condition to ramets growing in a light and saline water condition. We also hypothesized that ramets growing in heterogeneous environments achieve larger biomass than ramets in homogeneous environments. Ramets grown in light and saline conditions in heterogeneous environments allocated more biomass to aboveground parts, had taller shoots, larger Specific Green (leaf) Area and consumed less water than ramets grown in similar conditions but in a homogeneous environment. Results confirm the hypothesis that connected ramets in heterogeneous environments are specialised to capture locally abundant resources and share these with connected ramets growing in other habitats. The result of DoL is that the entire connected ramet system benefits and achieves higher biomass.     

Self-assembly,self-organization and division of labour

The prospect of generic principles of biological organization being uncovered through the increasingly broad use of the concepts of ''self-assembly'' and ''self-organization'' in biology will only be fulfilled if students of different levels of biological organization use the same terms with the same meanings. We consider the different ways the terms ''self-assembly'' and ''self-organization'' have been used, from studies of molecules to studies of animal societies. By linking ''self-assembly'' and ''self-organization'' with division of labour, we not only put forward a distinction between the underlying concepts but we are also able to relate them to the question: Why has a certain structure been favoured by natural selection? Using the particularly instructive case of social resilience in ant colonies, we demonstrate that the principle of self-organizing self-assembly may apply to higher levels of biological organization than previously considered. We predict that at the level of interactions among organisms within the most advanced animal societies, specialization through learning has a crucial role to play in re-assembly processes. This review may also help important commonalities and differences to be recognized between ordering mechanisms up to the social level and those further up the biological hierarchy, at the level of ecological communities.     

Colony size predicts division of labour in attine ants

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.     

Genetic and genomic analyses of the division of labour in insect societies

Division of labour--individuals specializing in different activities--features prominently in the spectacular success of the social insects. Until recently, genetic and genomic analyses of division of labour were limited to just a few species. However, research on an ever-increasing number of species has provided new insight, from which we highlight two results. First, heritable influences on division of labour are more pervasive than previously imagined. Second, different forms of division of labour, in lineages in which eusociality has arisen independently, have evolved through changes in the regulation of highly conserved molecular pathways associated with several basic life-history traits, including nutrition, metabolism and reproduction.     

Geometry explains the benefits of division of labour in a leafcutter ant

Many ant species have morphologically distinct worker sub-castes. This presumably increases colony efficiency and is thought to be optimized by natural selection. Optimality arguments are, however, often lacking in detail. In ants, the benefits of having workers in a range of sizes have rarely been explained mechanistically. In Atta leafcutter ants, large workers specialize in defence and also cut fruit. Fruit is soft and can be cut by smaller workers. Why, therefore, are large workers involved? According to the geometry hypothesis, cutting large pieces from three-dimensional objects like fruit is enhanced by longer mandibles. By contrast, long mandibles are not needed to cut leaves that are effectively two-dimensional. Our results from Atta laevigata support three predictions from the geometry hypothesis. First, larger workers cut larger fruit pieces. Second, the effect of large size is greater in cutting fruit than leaves. Third, the size of fruit pieces cut increases approximately in proportion to the cube of mandible length. Our results are a novel mechanistic example of how size variation among worker ants enhances division of labour.     

Response threshold reinforcements and division of labour in insect societies

A model of division of labour in insect societies, based on variable response thresholds is introduced. Response thresholds refer to the likelihood of reacting to task-associated stimuli. Low-threshold individuals perform tasks at a lower level of stimulus than high-threshold individuals. Within individual workers, performing a given task induces a decrease in the corresponding threshold, and not performing the task induces an increase in the threshold. This combined reinforcement process leads to the emergence of specialized workers, i.e. workers that are more responsive to stimuli associated with particular task requirements, from a group of initially identical individuals. Predictions of the dynamics of task specialization resulting from this model are presented. Predictions are also made as to what should be observed when specialists of a given task are removed from the colony and reintroduced after a varying amount of time: the colony does not recover the same state as that prior to the perturbation, and the difference between before and after the perturbation is more strongly marked as the time between separation and reintroduction increases.     

On the division of labour in the primitive termiteZootermopsis nevadensis (Hagen)

Conclusions It has been found that inZootermopsis nevadensis, a relatively primitive termite, the nymphs and older larvae carry out most nest-building behaviour, digging, and oscillatory movements. As they progress from young larvae to nymphs the termites tend to spend less time in trophallaxis and more time in other activities. The first instar nymphs and the sixth instar larvae are the most active in all respects. In terms of behaviour the sixth instar larvae are the nearest equivalent to a worker caste. Insects of the first nymphal instar can be roughly divided into those that spend much time in trophallaxis and relatively little in other activities andvice versa. This polarity was not evident in the younger insects.The replacement reproductives spend most of their time in trophallaxis and very little in other activities. Most of this trophallaxis is with the younger larvae, while most of the trophallaxis of the other instars is with the replacement reproductives. It is suggested that behavioural differences such as those found here may be important in caste determination and regulation.

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Résumé On a trouvé que chezZootermopsis nevadensis, termite relativement primitif, ce sont les nymphes et les plus vieilles larves qui manifestent le plus un comportement constructeur et exécutent la plupart du terrassement et des mouvements oscillatoires. En évoluant de l'état de jeunes larves à celui de nymphes, les termites ont tendance à passer moins de temps en trophallaxie et plus à d'autres activités. Les nymphes du premier stade et les larves du sixième stade sont les plus actives à tous points de vue.En termes de comportement, les larves du sixième stade sont l'équivalent le plus proche d'une caste d'ouvriers. Les nymphes du premier stade peuvent être, en gros, divisés en ceux qui passent beaucoup de temps en trophallaxie et relativement peu à d'autres activités et réciproquement. Cette polarité n'était pas évidente chez les insectes plus jeunes. Les sexués de remplacement passent la plupart de leur temps en trophallaxie et très peu à d'autres activités. La plus grande part de cette trophallaxie a lieu avec les plus jeunes larves, tandis que chez les autres stades elle a lieu avec les sexués de remplacement. Il est suggéré ici que les différences de comportement observées pourraient être importantes dans la détermination et la régulation des castes.

     

The reproductive division of labour in the queenless ponerine antRhytidoponera sp. 12

Summary Mated workers have replaced the queen as the functional egg-layers in several species of ponerine ants. In such queenless species, the reproductive status of workers can only be determined through ovarian dissections. However, the presence of yolky oocytes is not necessarily an indication of active egg-laying.InRhytidoponera sp. 12, a substantial proportion of the workers confined underground have many large yolky oocytes in their ovaries. Examination of various details of oogenesis (size and appearance of basal oocytes, ...) revealed that oocytes do not mature in unmated workers, and that they accumulate in the ovaries. In the 21 mated workers found in a colony excavated in October 1985, there were fewer large yolky oocytes, and the dense accumulations of yellow bodies indicated that eggs were laid regularly. Thus reproductive differentiation among the workers is controlled by insemination. The lack of egg-laying activity by unmated workers was confirmed by monitoring brood production in the laboratory. Trophic eggs do not seem to exist. Various characteristics of worker reproduction in ponerine ants are discussed.

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La division des rôles reproducteurs chez Rhytidoponera espèce 12, une fourmi Ponérine sans reine

Resume Des ouvrières fécondées ont remplacé la reine (dans sa fonction de pondeuse) chez plusieurs espèces de fourmis ponérines. Dans ces espèces sans reine, l'état reproductif des ouvrières ne peut être déterminé qu'avec la dissection des ovaires. Cependant, la présence d'ovocytes en vitellogenèse n'indique pas nécessairement qu'il y ait ponte d'ufs.ChezRhytidoponera espèce 12, une grande proportion des ouvrières actives à l'intérieur du nid ont beaucoup d'ovocytes en vitellogenèse dans leurs ovaires. L'examen de certains détails de l'ovogenèse (taille et apparence des ovocytes basaux...) a démontré que les ovocytes ne mûrissent pas chez les ouvrières non fécondées, et qu'ils s'accumulent dans les ovaires. Chez les 21 ouvrières fécondées trouvées dans une colonie déterrée en Octobre 1985, il y avait moins de gros ovocytes en vitellogenèse, et les accumulations denses de corps jaunes indiquaient que les ufs étaient pondus régulièrement. Donc la séparation des rôles parmi les ouvrières est contrôlée par la fécondation. L'absence de ponte par les ouvrières non fécondées a été confirmée par l'étude du développement du couvain dans des groupes de fourmis au laboratoire. Les ufs trophiques ne semblent pas exister. Certaines caractéristiques de la reproduction ouvrière chez les fourmis ponérines sont discutées.

     

Evolving the division of labour: generalists,specialists and task allocation

The evolutionary dynamics of specialization, in the context of the division of labour, are investigated. Individuals associate in groups in which benefits are shared and costs borne individually; each individual is either a generalist who can perform all the necessary tasks, a specialist who performs a sub-set of the necessary tasks, or a parasite who contributes nothing to the group. The implications of the model are explored analytically and through both numerical and Monte Carlo methods. These methods demonstrate the evolution of populations towards stable arrangements of specialists and generalists. The fittest populations are those that divide tasks fairly and associate in large, highly specialized groups. Generalists have a distinct advantage in small groups, but the presence of generalists, ironically, lowers group fitness. Parasites are able to invade both specialized and non-specialized populations. A basic model for the continuous division of labour is also presented, demonstrating a tendency for populations to evolve increasingly unfair divisions of labour. This last result implies that an evolutionary ratchet favours disparity between the workload of specialist populations.     

Ants in a labyrinth: a statistical mechanics approach to the division of labour

Division of labour (DoL) is a fundamental organisational principle in human societies, within virtual and robotic swarms and at all levels of biological organisation. DoL reaches a pinnacle in the insect societies where the most widely used model is based on variation in response thresholds among individuals, and the assumption that individuals and stimuli are well-mixed. Here, we present a spatially explicit model of DoL. Our model is inspired by Pierre de Gennes' 'Ant in a Labyrinth' which laid the foundations of an entire new field in statistical mechanics. We demonstrate the emergence, even in a simplified one-dimensional model, of a spatial patterning of individuals and a right-skewed activity distribution, both of which are characteristics of division of labour in animal societies. We then show using a two-dimensional model that the work done by an individual within an activity bout is a sigmoidal function of its response threshold. Furthermore, there is an inverse relationship between the overall stimulus level and the skewness of the activity distribution. Therefore, the difference in the amount of work done by two individuals with different thresholds increases as the overall stimulus level decreases. Indeed, spatial fluctuations of task stimuli are minimised at these low stimulus levels. Hence, the more unequally labour is divided amongst individuals, the greater the ability of the colony to maintain homeostasis. Finally, we show that the non-random spatial distribution of individuals within biological and social systems could be caused by indirect (stigmergic) interactions, rather than direct agent-to-agent interactions. Our model links the principle of DoL with principles in the statistical mechanics and provides testable hypotheses for future experiments.