The fitness consequences of bearing domatia and having the right ant partner: experiments with protective and non-protective ants in a semi-myrmecophyte

The fitness advantage provided by caulinary domatia to myrmecophytes has never been directly demonstrated because most myrmecophytic species do not present any individual variation in the presence of domatia and the removal of domatia from entire plants is a destructive process. The semi-myrmecophytic tree, Humboldtia brunonis (Fabaceae: Caesalpinioideae), is an ideal species to investigate the selective advantage conferred by domatia because within the same population, some plants are devoid of domatia while others bear them. Several ant species patrol the plant for extra-floral nectar. Fruit production was found to be enhanced in domatia-bearing trees compared to trees devoid of domatia independent of the ant associate. However, this domatium effect was most conspicuous for trees associated with the populous and nomadic ant, Technomyrmex albipes. This species is a frequent associate of H. brunonis, inhabiting its domatia or building carton nests on it. Ant exclusion experiments revealed that T. albipes was the only ant to provide efficient anti-herbivore protection to the leaves of its host tree. Measures of ant activity as well as experiments using caterpillars revealed that the higher efficiency of T. albipes was due to its greater patrolling density and consequent shorter lag time in attacking the larvae. T. albipes also provided efficient anti-herbivore protection to flowers since fruit initiation was greater on ant-patrolled inflorescences than on those from which ants were excluded. We therefore demonstrated that caulinary domatia provide a selective advantage to their host-plant and that biotic defence is potentially the main fitness benefit mediated by domatia. However, it is not the sole advantage. The general positive effect of domatia on fruit set in this ant-plant could reflect other benefits conferred by domatia-inhabitants, which are not restricted to ants in this myrmecophyte, but comprise a large diversity of other invertebrates. Our results indicate that mutualisms enhance the evolution of myrmecophytism

A viscoelastic deadly fluid in carnivorous pitcher plants

Background : The carnivorous plants of the genus Nepenthes, widely distributed in the Asian tropics, rely mostly on nutrients derived from arthropods trapped in their pitcher-shaped leaves and digested by their enzymatic fluid. The genus exhibits a great diversity of prey and pitcher forms and its mechanism of trapping has long intrigued scientists. The slippery inner surfaces of the pitchers, which can be waxy or highly wettable, have so far been considered as the key trapping devices. However, the occurrence of species lacking such epidermal specializations but still effective at trapping insects suggests the possible implication of other mechanisms. Methodology/Principal Findings : Using a combination of insect bioassays, high-speed video and rheological measurements, we show that the digestive fluid of Nepenthes rafflesiana is highly viscoelastic and that this physical property is crucial for the retention of insects in its traps. Trapping efficiency is shown to remain strong even when the fluid is highly diluted by water, as long as the elastic relaxation time of the fluid is higher than the typical time scale of insect movements. Conclusions/Significance : This finding challenges the common classification of Nepenthes pitchers as simple passive traps and is of great adaptive significance for these tropical plants, which are often submitted to high rainfalls and variations in fluid concentration. The viscoelastic trap constitutes a cryptic but potentially widespread adaptation of Nepenthes species and could be a homologous trait shared through common ancestry with the sundew (Drosera) flypaper plants. Such large production of a highly viscoelastic biopolymer fluid in permanent pools is nevertheless unique in the plant kingdom and suggests novel applications for pest control

Social and Hydrological Responses to Extreme Precipitations: An Interdisciplinary Strategy for Postflood Investigation

International audienceThis paper describes and illustrates a methodology to conduct postflood investigations based on interdisciplinary collaboration between social and physical scientists. The method, designed to explore the link between crisis behavioral response and hydrometeorological dynamics, aims at understanding the spatial and temporal capacities and constraints on human behaviors in fast-evolving hydrometeorological conditions. It builds on methods coming from both geosciences and transportations studies to complement existing post-flood field investigation methodology used by hydrometeorologists. The authors propose an interview framework, structured around a chronological guideline to allow people who experienced the flood firsthand to tell the stories of the circumstances in which their activities were affected during the flash flood. This paper applies the data collection method to the case of the 15 June 2010 flash flood event that killed 26 people in the Draguignan area (Var, France). As a first step, based on the collected narratives, an abductive approach allowed the identification of the possible factors influencing individual responses to flash floods. As a second step, behavioral responses were classified into categories of activities based on the respondents' narratives. Then, aspatial and temporal analysis of the sequences made of the categories of action to contextualize the set of coping responses with respect to local hydrometeorological conditions is proposed. During this event, the respondents mostly follow the pace of change in their local environmental conditions as the flash flood occurs, official flood anticipation being rather limited and based on a large-scale weather watch. Therefore, contextual factors appear as strongly influencing the individual's ability to cope with the event in such a situation

Range Expansion Drives Dispersal Evolution In An Equatorial Three-Species Symbiosis

A-09-14International audienceBackground Recurrent climatic oscillations have produced dramatic changes in species distributions. This process has been proposed to be a major evolutionary force, shaping many life history traits of species, and to govern global patterns of biodiversity at different scales. During range expansions selection may favor the evolution of higher dispersal, and symbiotic interactions may be affected. It has been argued that a weakness of climate fluctuation-driven range dynamics at equatorial latitudes has facilitated the persistence there of more specialized species and interactions. However, how much the biology and ecology of species is changed by range dynamics has seldom been investigated, particularly in equatorial regions. Methodology/Principal Findings We studied a three-species symbiosis endemic to coastal equatorial rainforests in Cameroon, where the impact of range dynamics is supposed to be limited, comprised of two species-specific obligate mutualists –an ant-plant and its protective ant– and a species-specific ant parasite of this mutualism. We combined analyses of within-species genetic diversity and of phenotypic variation in a transect at the southern range limit of this ant-plant system. All three species present congruent genetic signatures of recent gradual southward expansion, a result compatible with available regional paleoclimatic data. As predicted, this expansion has been accompanied by the evolution of more dispersive traits in the two ant species. In contrast, we detected no evidence of change in lifetime reproductive strategy in the tree, nor in its investment in food resources provided to its symbiotic ants. Conclusions/Significance Despite the decreasing investment in protective workers and the increasing investment in dispersing females by both the mutualistic and the parasitic ant species, there was no evidence of destabilization of the symbiosis at the colonization front. To our knowledge, we provide here the first evidence at equatorial latitudes that biological traits associated with dispersal are affected by the range expansion dynamics of a set of interacting species

Protection against herbivores of the myrmecophyte Leonardoxa africana (Baill.) Aubrèv. T3 by its principal ant inhabitant Aphomomyrmex afer Emery

International audienceLeonardoxa africana T3 is a myrmecophyte, a plant with specialized struc- tures (domatia) that shelter ants. Adult trees are essentially all occupied by the ant Apho- momyrmex afer. One tree possesses one ant colony. Ants tend homopterans inside the domatia. The plant provides ants with nest sites and food via production of extrafloral nectar and via honeydew produced by homopterans. Workers patrol the young leaves, although their nectaries are not yet functional. This study was conducted to investigate the nature of the relationship between the plant and its ants. In order to determine whether ants protect the plant against herbivorous insects, we placed microlepidopteran larvae on young leaves of several trees, and measured the time until discovery of the larvae by the workers. We then studied the responses of workers as a function of insect size. We showed that workers patrolled the young leaves of the majority of trees. There was, however, inter-colony variability in intensity of patrolling. Workers attacked every larva they found, killing and eating the smaller ones, and chasing larger ones off the young leaf. Most of the phytophagous insects attacking young leaves of L. africana T3 were inventoried in this study. We showed that the larvae of microlepidopterans, one of the most important herbivores of this species, form part of the diet of A. afer. The function of the stereotyped behaviour of ant patrolling on young leaves may be in part to obtain insect protein to complement carbohydrate-rich nectar and honeydew, and in part to protect the host and thus increase its production of resources for ants. Our study shows that ants protect the tree against herbivores, and that even if this protection is less pronounced and more variable than that demonstrated for their sister species L. africana sensu stricto and Petalomyrmex phylax, the association between L. africana T3 and A. afer is a mutualism. ( Académie des sciences / Elsevier, Paris.

InsectChange: Comment

The InsectChange database (van Klink et al. 2021) underlying the meta-analysis by van Klink et al. (2020a) compiles worldwide time series of abundance and biomass of invertebrates reported as insects and arachnids, as well as ecological data likely to influence their change. Based on a comprehensive review of the original publications and datasets, we highlight numerous issues in this database, such as errors in insect counts, sampling biases, inclusion of non-insects driving assemblage trends, omission of internal drivers investigated in the original studies and inaccurate assessment of local cropland cover. We argue that in its current state this database does not allow to study the temporal trends of insects or their drivers. Our in-depth analysis therefore calls for major changes and extreme vigilance in its use. It precisely details each problem identified and makes numerous suggestions for improvement in the supplementary information, which can be used as a basis for corrections

How identity of the homopteran trophobiont affects sex allocation in a symbiotic plant-ant: the proximate role of food

International audienceWe provide evidence for the proximate role of food in sex allocation by an ant species, and demonstrate how identity of the homopteran partner affects benefits to colonies of a plant-symbiotic ant. The system studied includes a plant-ant that nests in swollen hollowed internodes of a myrmecophyte, and two species of homopteran trophobionts (a coccid and a pseudococcid) tended inside domatia by these ants, for which they are an essential source of food. Total investment in pupae was greater for ant colonies that tended solely or primarily coccids than for those that tended pseudococcids. In particular, biomass invested in sexuals increased more rapidly with size of the colony in trees where ants tended coccids. This greater investment in sexuals was not made at the expense of investment in workers, but reflected increased resources available to coccid-tending colonies. Higher reproductive output indicates that ant fitness may be greater when they tend coccids. These additional resources led to a greater increase in production of alate females than in that of males. Consequently, the sex investment ratio of coccid-tending colonies was more female biased than in those that tended pseudococcids. Differences in resource supply affected numbers of individuals produced but not per-individual investment, with one partial exception: in very small colonies, pseudococcid-tending colonies produced small workers while coccid-tending colonies did not, further underlining the higher resource supply to coccid-tending colonies. This study provides evidence for the proximate role played by food in sex allocation at the colony level. We discuss our results in the context of hypotheses aimed at explaining sex ratio at the colony and population levels

An Ant-Plant Mutualism and Its Host-Specific Parasite: Activity Rhythms, Young Leaf Patrolling, and Effects on Herbivores of Two Specialist Plant-Ants Inhabiting the Same Myrmecophyte

International audienceLeonardoxa africana is an understorey tree of the coastal rainforests of Cameroon that provides food (extrafloral nectar) and nest sites (swollen, hollowed internodes) for ants. Only two host-specific species of ants inhabit this tree. The present study showed that their distributions were mutually exclusive: the formicine ant Petalomyrmex phylax inhabited three-fourths of all occupied trees, while the myrmicine Cataulacus mckeyi occupied the remaining trees. In order to determine whether the presence of each of these ants was beneficial to the trees, we compared rates of damage on young leaves patrolled by ants and on young leaves from which ants were experimentally excluded. We also studied activity rhythms of the two ants and their responses to phytophagous insects they encountered. Young leaves patrolled by Petalomyrmex suffered significantly less damage than those from which ants were excluded (2% versus 24%). In contrast, young leaves patrolled by Cataulacus suffered much greater herbivory (31%) than those patrolled by Petalomyrmex, and herbivory on ant-patrolled leaves was not significantly different from that on ant-excluded leaves (46%). Behavioural observations help to explain the difference between the effects of the two ant species. Number of workers active on plant surfaces was much greater on Petalomyrmex-occupied trees than on trees occupied by Cataulacus. Petalomyrmex workers patrolled young leaves constantly (day and night) and chased out or killed microlepidopteran larvae placed on young leaves. The patrolling activity of Cataulacus was only diurnal (rather well correlated with the activity of nectar production), and Cataulacus workers failed to consistently attack herbivores. These results confirm that Petalomyrmex is a mutualist of Leonardoxa and demonstrate that Cataulacus, exploiting the resources of its host, providing no protection and excluding the mutualist from trees it occupies, is a parasite of the mutualism. We discuss origin, ecological persistence and evolutionary stability of such a parasitic strategy in plant-ant symbioses, and we ask whether mutualisms may evolve from such parasitic relationships

Ant-plant conflicts and a novel case of castration parasitism in a myrmecophyte

Questions: Do protective plant-ants perturb the pollination process and the reproduction of their host-plant? If they do, have partner selective mechanisms evolved against such conflicts? Organisms: The semi-myrmecophyte Humboldtia brunonis and its ant associates. Field site: Makut Reserve Forest, Western Ghats. South India. Methods: We tracked insect and extrafloral nectar activity on inflorescences of several trees over a 24 h cycle. We repeatedly measured the extrafloral nectar produced by bracts of flowers throughout their phenology from the bud stage until and beyond flower opening. We studied the behaviour of ants towards the reproductive apparatus of the flowers and conducted ant exclusion experiments to test for my negative effect on herbivores of fruit production. Conclusions: Pollinators did not visit inflorescences that had more than four ants on them. Ants. solely by their presence on bud bracts and bracteoles. intimidate other insects, both pollinators and herbivores. Some spatial and temporal mechanisms partially prevent negative ant-pollinator interactions. First. extrafloral nectar production on the bracts of flower buds, which attracts ants to inflorescences. was highest at night, attracting the largest numbers of ants at that time, whereas the major pollinators were active during the day. Second, this extrafloral nectar production declines after the first flower of each inflorescence opens. Third, the anthers and stigma are placed at the apex of a thin elongate axis, which offers a precarious foothold to ants. One ant species, Crematogaster dohrni, succeeds despite these difficulties by acting just before the flower-opens, and damaging the flower when the style and stamens are still folded. This is the fourth case of castration behaviour of a plant-ant directed against its host-plant. Despite its anti-herbivore protection of flower buds. this plant-ant has a negative impact on fruit production in H. brunonis