Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries

Many plants secrete nectar from extrafloral nectaries (EFNs), specialized structures that usually attract ants which can act as plant defenders. We examined the nectar-mediated interactions between Chamaecrista nictitans (Caesalpineaceae) and jumping spiders (Araneae, Salticidae) for 2 years in old fields in New Jersey, USA. Previous research suggests that spiders are entirely carnivorous, yet jumping spiders (Eris sp. and Metaphidippus sp.) on C. nictitans collected nectar in addition to feeding on herbivores, ants, bees, and other spiders. In a controlled-environment experiment, when given a choice between C. nictitans with or without active EFNs, foraging spiders spent 86% of their time on plants with nectar. C. nictitans with resident jumping spiders did set significantly more seed than plants with no spiders, indicating a beneficial effect from these predators. However, the presence of jumping spiders did not decrease numbers of Sennius cruentatus (Bruchidae), a specialist seed predator of C. nictitans. Jumping spiders may provide additional, unexpected defense to plants possessing EFNs. Plants with EFNs may therefore have beneficial interactions with other arthropod predators in addition to nectar-collecting ants. Received: 27 May 1998 / Accepted: 23 December 1998     

Emergent Impacts of Ant and Spider Interactions: Herbivory Reduction in a Tropical Savanna Tree

Multiple predators often have effects on their common prey populations that cannot be predicted by summing the effects of each predator at a time. When predators forage on the same vegetation substrate, intraguild interactions might cause emergent outcomes for the plants on which the predators co‐occur. We experimentally evaluated the effects of spiders and ants on herbivory and reproduction in the extrafloral nectary‐bearing tree Qualea multiflora (Vochysiaceae). Plants were divided in four experimental groups, depending on the presence or absence of ants and spiders. We compared the effects of each treatment on richness and abundance of chewing and sucking herbivores and on herbivory (leaf area loss). We also evaluated the impact of predators on the production of buds, fruits and seeds, and weight of the fruits. The presence of ants reduced the abundance and richness of spiders, but spiders did not affect the abundance and richness of ants. Only the removal of ants resulted in a significant increase in the abundance of herbivores and herbivore richness. Herbivory, however, was also affected by spiders. In addition, we found a significant interaction effect of ants and spiders on herbivory, indicating an emergent multiple predator effect. Neither ants nor spiders had an impact on the number of buds produced, number of fruits per bud, and seeds per fruits or fruit weight. This study highlights the importance of evaluating the effect of the predator fauna as a whole and not only one specific group on herbivory.     

Florivorous myrmecophilous caterpillars exploit an ant–plant mutualism and distract ants from extrafloral nectaries

Females of myrmecophilous butterflies tend to oviposit in plants visited by ant species that engage in stable associations with its larvae. In Banisteriopsis malifolia, caterpillars are attended by the same ants that feed on extrafloral nectaries. A conflict may arise when both the plant and caterpillars compete for ant attention, and ants are assumed to forage on the highest quality resource. By attending caterpillars, ants can be indirectly detrimental to plant fitness because florivorous larvae feed intensively until pupation. In this study, we specifically investigated (i) whether the occurrence of facultative myrmecophilous Synargis calyce (Riodinidae) caterpillars in B. malifolia was based on ant species (Camponotus blandus or Ectatomma tuberculatum) and abundance; (ii) the monopolization of ants by the butterfly larvae and (iii) the florivory rates incurred by the caterpillars on inflorescences. The abundance of S. calyce was six‐fold greater in plants with C. blandus, compared to E. tuberculatum treatments. Caterpillars monopolized up to 50% of C. blandus on the plants, indicating that the resources offered by S. calyce were more attractive to ants than extrafloral nectaries. Florivory by riodinids incurred losses of almost 60% of flower buds. Myrmecophilous riodinids exploited an ant–plant mutualism by attracting aggressive ants that become larvae bodyguards. Thus, this ecological interaction is potentially detrimental to B. malifolia, since the ants, which can provide protection against herbivores, shift to provide defence for one of these herbivores.     

Foraging behavior of Brachygastra lecheguana (Hymenoptera: Vespidae) on Banisteriopsis malifolia (Malpighiaceae): Extrafloral nectar consumption and herbivore predation in a tending ant system

In the Brazilian savanna many plant species bear regular associations with patrolling ants that are aggressive towards insect herbivores. However, not only ants but also several species of predatory wasps are attracted to plants due to the extrafloral nectaries (EFNs). Such wasps feed on both herbivores and plant exudates. In this study we describe the foraging behavior of the social Polistinae wasp Brachygastra lecheguana in the extrafloral nectaried shrub Banisteriopsis malifolia, and investigated the influence of patrolling ants Camponotus blandus on the activity of the wasp. Brachygastra lecheguana fed on the endophytic larvae of Anthonomus (Curculionidae) beetles that developed inside flower buds. The wasp lacerated the bud layers to reach the beetle larvae located at the bud core. The wasp visits to Ba. malifolia were statistically related to the abundance of flower buds and beetles. Ant exclusion experiments revealed that the hunting behavior of B. lecheguana on beetles was not related to the absence of C. blandus. However we found that wasps spent more time consuming extrafloral nectar on branches where ants were excluded. This is the first study reporting extrafloral nectar consumption by B. lecheguana, as well as the predation on herbivores in natural areas. In cerrado vegetation, ants benefit the plant by reducing insect herbivores, and our study provides evidence that the B. lecheguana – Ba. malifolia system represents a potential interaction where the wasp may also benefit the host plant. The value of this wasp species as a plant‐guard is discussed.     

Non‐trophic effects of litter reduce ant predation and determine caterpillar survival and distribution

The tritrophic model featuring plants consumed by herbivores consumed by parasitoids or predators has become the primary paradigm used to describe herbivore dynamics. However, interactions involving herbivores can be habitat‐ specific and plants often provide habitat, as well as food. Structural complexity of the habitat may favor predators or may allow herbivore prey to escape detection and capture. This study considered the spatial and temporal dynamics of an arctiid caterpillar, Platyprepia virginalis. The tritrophic model that includes only a tachinid parasitoid that attacks P. virginalis and the caterpillars’ primary host‐plant, Lupinus arboreus, has failed to provide much insight into this system. Instead, we found that ants killed and removed many small caterpillars. Protecting caterpillars from ants increased their survival three‐fold and five‐fold in assays conducted during two years. Caterpillars were more likely to survive in short‐term assays at sites that naturally had a deeper cover of dead and living plant material. Experiments with baits showed that ant recruitment declined as litter depth increased on average. These survey results indicated that ant predation was an important source of mortality for young caterpillars and that the presence of thick litter reduced this mortality. These results were corroborated in an experiment that manipulated litter depth and ant access to caterpillars. Previous findings that other defoliating caterpillars increased litter depth and benefitted P. virginalis are also consistent with this hypothesis. Litter acts as an important non‐trophic resource, allowing caterpillars to avoid predation by ants such that wet sites with deep litter act as source populations for caterpillars. Our results show strong effects of both trophic and non‐trophic interactions since plants indirectly provided limiting habitat and this heterogeneous habitat strongly affected risk of predation and ultimately caterpillar abundance and distribution.     

Seed predators are undeterred by nectar-feeding ants on Chamaecrista nictitans (Caesalpineaceae)

There are many examples of mutualistic interactions between ants and plants bearing extrafloral nectaries (EFN). The annual legume Chamaecrista nictitans (Caesalpineaceae) secretes nectar from EFN, specialized structures that attract ants, spiders, and other arthropods. The effects of manipulated C. nictitans patch size and location on plant-ant interactions were tested. Defense from herbivores was not detected; plants with ants did not set significantly more fruit or seed than plants with ants excluded. On the contrary, in one year, plants without ants set more fruit and seed than C. nictitans with ants. The cause of this was not determined. Furthermore, insect herbivore damage was low during three years of observations. Sennius cruentatus (Bruchidae), a specialist seed predator beetle, escaped ant defense despite the presence of numerous ants. Beetle progeny are protected during development by living inside maturing C. nictitans fruit and preventing fruits from dehiscing before emerging as adults. Although ants reduced percent of infestation in 1995, the total number of S. cruentatus per plant was not affected by ants in years of infestation. Overall, larger experimental C. nictitans patches attracted more ants, parasitoid wasps, and percent infestation by S. cruentatus while insect herbivores declined with increasing patch size. Location of patches within fields, however, did not affect numbers of arthropod visitors. Similar to manipulated populations, very little insect herbivory occurred in four reference populations. In contrast to the experimental populations, no S. cruentatus were recovered in reference populations of C. nictitans. Herbivory by insects may not always depress seed set by C. nictitans or may not exceed a threshold level. Thus, herbivory-reduction by ants may not have been detectable in these results. Seed predation may be more influential on C. nictitans reproduction. This revised version was published online in August 2006 with corrections to the Cover Date.     

The effect of disturbance on an ant–plant mutualism

Protective ant–plant mutualisms—where plants provide food or shelter to ants and ants protect the plants from herbivores—are a common feature in many ecological communities, but few studies have examined the effect of disturbance on these interactions. Disturbance may affect the relationship between plants and their associated ant mutualists by increasing the plants’ susceptibility to herbivores, changing the amount of reward provided for the ants, and altering the abundance of ants and other predators. Pruning was used to simulate the damage to buttonwood mangrove (Conocarpus erectus) caused by hurricanes. Pruned plants grew faster than unpruned plants, produced lower levels of physical anti-herbivore defenses (trichomes, toughness), and higher levels of chemical defenses (tannins) and extrafloral nectaries. Thus, simulated hurricane damage increased plant growth and the amount of reward provided to ant mutualists, but did not have consistent effects on other anti-herbivore defenses. Both herbivores and ants increased in abundance on pruned plants, indicating that the effects of simulated hurricane damage on plant traits were propagated to higher trophic levels. Ant-exclusion led to higher leaf damage on both pruned and upruned plants. The effect of ant-exclusion did not differ between pruned and unpruned plants, despite the fact that pruned plants had higher ant and herbivore densities, produced more extrafloral nectaries, and had fewer physical defenses. Another common predator, clubionid spiders, increased in abundance on pruned plants from which ants had been excluded. I suggest that compensatory predation by these spiders diminished the effect of ant-exclusion on pruned plants.     

Sugar secretion and ant protection in Ficus benguetensis: Toward a general trend of fig–ant interactions

The relationship between plants and ants is often mediated by the presence of extrafloral nectaries (EFNs) that attract ants and provide rewards by protecting plants from herbivores or parasites. Ficus trees (Moraceae) and their pollinators (Hymenoptera: Agaonidae) are parasitized by many nonpollinating fig wasp species (Hymenoptera: Chalcidoidea) that decrease the reproductive output of the mutualistic partners. Previous studies have shown that ants living on and patrolling Ficus species can efficiently deter parasitic wasps. The aim of this study was to verify the presence of EFNs on figs of Ficus benguetensis and test the hypothetical protection service provided by ants. Figs in different developmental stages were collected from Fu-Yang Eco Park, Taipei, Taiwan. Sugars on the fig surface were collected and analyzed through high-performance anion-exchange chromatography. Moreover, ants were excluded from the figs to determine the effect of ants on the nonpollinating fig wasps. We identified three oligosaccharides whose relative proportions varied with the fig developmental phase. In addition, results showed that the ant-excluded figs were heavily parasitized and produced three times less pollinators than did the control figs. Finally, the specific interactions of Ficus benguetensis with ants and the relationship between figs and ants in general are discussed.     

Temporal and geographic variation in parasitoid attack with no evidence for ant protection of the Melissa blue butterfly,Lycaeides melissa

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Life tables for the guava psyllid Triozoida limbata in southeastern Brazil

The aim of this study was to identify, quantify, and determine the importance of biological control agents of the psyllid Triozoida limbata (Enderlein) (Hemiptera: Sternorrhyncha: Triozidae). Ecological life tables were developed during four periods to determine the critical stage and key mortality factors of this pest. Predation and parasitism were found to be the two major factors driving the population dynamics of this pest. The major predators of eggs and nymphs of first and second instars were coccinellids, predatory thrips, lacewings, ants, and spiders, while the major predators of third, fourth, and fifth instars were several species of predatory wasps and syrphids. The endoparasitoid Psyllaephagus sp. (Hymenoptera: Encyrtidae) parasitized fifth instar psyllids. The fifth instar was found to be the critical mortality stage of T. limbata, and key mortality factors include the parasitoid Psyllaephagus sp. and predatory wasps.     

Behavioural ecology of defence in a risky environment: caterpillars versus ants in a Neotropical savanna

1. Predatory ants may reduce infestation by herbivorous insects, and slow‐moving Lepidopteran larvae are often vulnerable on foliage. We investigate whether caterpillars with morphological or behavioural defences have decreased risk of falling prey to ants, and if defence traits mediate host plant use in ant‐rich cerrado savanna. 2. Caterpillars were surveyed in four cerrado localities in southeast Brazil (70–460 km apart). The efficacy of caterpillar defensive traits against predation by two common ant species (Camponotus crassus, C. renggeri) was assessed through experimental trials using caterpillars of different species and captive ant colonies. 3. Although ant presence can reduce caterpillar infestation, the ants' predatory effects depend on caterpillar defence traits. Shelter construction and morphological defences can prevent ant attacks (primary defence), but once exposed or discovered by ants, caterpillars rely on their size and/or behaviour to survive (secondary defence). 4. Defence efficiency depends on ant identity: C. renggeri was more aggressive and lethal to caterpillars than C. crassus. Caterpillars without morphological defences or inside open shelters were found on plants with decreased ant numbers. No unsheltered caterpillar was found on plants with extrafloral nectaries (EFNs). Caterpillars using EFN‐bearing plants lived in closed shelters or presented morphological defences (hairs, spines), and were less frequently attacked by ants during trials. 5. The efficiency of defences against ants is thus crucial for caterpillar survival and determines host plant use by lepidopterans in cerrado. Our study highlights the effect of EFN‐mediated ant‐plant interactions on host plant use by insect herbivores, emphasizing the importance of a tritrophic viewpoint in risky environments.     

Fire triggers the activity of extrafloral nectaries,but ants fail to protect the plant against herbivores in a neotropical savanna

Herbivores are attracted to young shoots and leaves because of their tender tissues. However, in extrafloral nectaried plants, young leaves also attract patrolling ants, which may chase or prey on herbivores. We examined this scenario in extrafloral nectaried shrubs of Banisteriopsis malifolia resprouting after fire, which promoted both the aseasonal production of leaves and the activity of extrafloral nectaries (EFNs). Results were compared between resprouting (burned) and unburned control plants. The aggressive ant species Camponotus crassus and the herbivorous thrips Pseudophilothrips obscuricornis were respectively rapidly attracted to resprouting plants because of the active EFNs and their less sclerophyllous leaves. The abundance of these insects was almost negligible in the control (unburned) shrubs. Ants failed to protect B. malifolia, as no thrips were preyed upon or injured by ants in resprouting plants. Consequently, on average, 37 % of leaves from resprouting shrubs had necrosis marks. Upon contact with ants, thrips released small liquid droplets from their abdomen, which rapidly displaced ants from the surroundings. This study shows that P. obscuricornis disrupted the facultative mutualism between C. crassus and B. malifolia, since ants received extrafloral nectar from plants, but were unable to deter herbivore thrips.     

Density Patterns of Piper Ant-Plants and Associated Arthropods: Top-Predator Trophic Cascades in a Terrestrial System?1

Top-predator (fourth-trophic-level) controlled trophic cascades are thought to be uncommon in terrestrial systems, but actual quantitative tests and comparisons of bottom-up and top-down forces in systems with more than three linear trophic levels are rare. Here, we describe the density patterns of the arthropod community associated with Piper ant-plants in Costa Rican wet forests. Consumers in this community comprise a complex, interacting web of herbivores, predaceous ants, and predators of ants. Although the hollow stems and petioles of the Piper plants provide some protection to resident ants from predation, specialized Dipoena spiders and Phyllobaenus beetles exploit Pheidole ants inhabiting Piper plants. We report abundance patterns of plants, ants and predators in four forests. These patterns of abundance are consistent with predictions of top-down cascades across four trophic levels when the top predators are effective (beetles). We discuss how top-down and bottom-up forces may interact in systems with less effective top predators (spiders).     

FOSSIL EXTRAFLORAL NECTARIES,EVIDENCE FOR THE ANT-GUARD ANTIHERBIVORE DEFENSE IN AN OLIGOCENE POPULUS

Extrafloral nectaries are secretory glands, usually found on leaves, that have been shown to promote ant defense against the insect herbivores of many modem day plants. Extrafloral nectaries were found on the 35-million-year-old fossil leaves of the extinct Populus crassa from Florissant, Colorado. Extinct ant species (belonging to five still extant genera that have modem ant-guard species), and other predators and parasitoids (whose modem relatives frequent extrafloral nectaries) also lived at Florissant. The extrafloral nectaries of P. crassa (and perhaps other plants) probably operated to attract ants and/or other arthropod defenders as early as the Oligocene.     

Does leaf ontogeny lead to changes in defensive strategies against insect herbivores?

Plants use different defense strategies throughout their ontogenetic development. In this study, three questions were proposed: (1) Is there a greater abundance of ants on young leaves, which possess active extrafloral nectaries, than on mature leaves? (2) Do ants exert an indirect defense that is effective against the attack of herbivorous insects? (3) Do mature leaves have a greater concentration of physical and chemical defense than young leaves? These questions were addressed through an ant-exclusion experiment in which two branches of Copaifera langsdorffii (n = 25) were marked and monitored throughout the entire foliar expansion and development period. A reduction in the abundance of ants throughout foliar development was observed. The ants exerted an effective defense against herbivores on C. langsdorffii: the branches where ants were excluded had a greater number of herbivores. The mature leaves possessed a greater index of leaf sclerophylly than young leaves, but the leaves did not differ in the concentration of tannins. The foliar ontogeny of C. langsdorffii promoted an inversion in the defense strategy against herbivores, and despite showing an opportunistic relationship, the interaction between ants and extrafloral nectaries appears to play an important role in structuring the interactions between herbivorous insects and their host plants.     

Behavioral strategy of a lycaenid (Lepidoptera) caterpillar against aggressive ants in a Brazilian savanna

Myrmecophily is widespread in lycaenid butterflies, in which ants receive food resources and, in turn, protect caterpillars against natural enemies. This interaction ranges from obligate myrmecophily, in which immatures are invariably associated with ants and are dependent on ants for survival, and facultative myrmecophily, in which larvae are not dependent on ants for survival, but the presence of the latter may increase larvae survival. Lycaenids also include non-myrmecophilous butterflies, which do not have positive associations with ants and have developed strategies to avoid being attacked or preyed upon by them. In this study, we examined the relationship between the lycaenid Michaelus ira and two ant species associated with Distictella elongata (Bignoniaceae). This plant has extrafloral nectaries and is patrolled by Camponotus crassus and Ectatomma tuberculatum. Morphological analyses revealed that M. ira larvae have ant organs, such as dorsal nectary organs and perforated cupolas, structures associated with myrmecophily. We performed larval exposure experiments in the field, predicting that, in the absence of myrmecophily, the butterfly larva would present strategies to avoid ant attack. Results showed that larvae were attacked by both ant species. To escape ant molestation, larvae lived and fed inside silk-sealed D. elongata flower buds. We concluded that the M. ira bud-sheltering behavior was a defensive strategy against these ant species, while the dorsal nectary organs were apparently nonfunctional. Nonetheless, myrmecophily, in general, cannot be excluded in M. ira since relationships with other ant species may exist.     

Geographic variation in a facultative mutualism: consequences for local arthropod composition and diversity

Geographic variation in the outcome of interspecific interactions may influence not only the evolutionary trajectories of species but also the structure of local communities. We investigated this community consequence of geographic variation for a facultative mutualism between ants and wild cotton (Gossypium thurberi). Ants consume wild cotton extrafloral nectar and can protect plants from herbivores. We chose three sites that differed in interaction outcome, including a mutualism (ants provided the greatest benefits to plant fitness and responded to manipulations of extrafloral nectar), a potential commensalism (ants increased plant fitness but were unresponsive to extrafloral nectar), and a neutral interaction (ants neither affected plant fitness nor responded to extrafloral nectar). At all sites, we manipulated ants and extrafloral nectar in a factorial design and monitored the abundance, diversity, and composition of other arthropods occurring on wild cotton plants. We predicted that the effects of ants and extrafloral nectar on arthropods would be largest in the location with the mutualism and weakest where the interaction was neutral. A non-metric multidimensional scaling analysis revealed that the presence of ants altered arthropod composition, but only at the two sites in which ants increased plant fitness. At the site with the mutualism, ants also suppressed detritivore/scavenger abundance and increased aphids. The presence of extrafloral nectar increased arthropod abundance where mutual benefits were the strongest, whereas both arthropod abundance and morphospecies richness declined with extrafloral nectar availability at the site with the weakest ant–plant interaction. Some responses were geographically invariable: total arthropod richness and evenness declined by approximately 20% on plants with ants, and extrafloral nectar reduced carnivore abundance when ants were excluded from plants. These results demonstrate that a facultative ant–plant mutualism can alter the composition of arthropod assemblages on plants and that these community-level consequences vary across the landscape.     

Synergistic effects of direct and indirect defences on herbivore egg survival in a wild crucifer

Evolutionary theory of plant defences against herbivores predicts a trade-off between direct (anti-herbivore traits) and indirect defences (attraction of carnivores) when carnivore fitness is reduced. Such a trade-off is expected in plant species that kill herbivore eggs by exhibiting a hypersensitive response (HR)-like necrosis, which should then negatively affect carnivores. We used the black mustard (Brassica nigra) to investigate how this potentially lethal direct trait affects preferences and/or performances of specialist cabbage white butterflies (Pieris spp.), and their natural enemies, tiny egg parasitoid wasps (Trichogramma spp.). Both within and between black mustard populations, we observed variation in the expression of Pieris egg-induced HR. Butterfly eggs on plants with HR-like necrosis suffered lower hatching rates and higher parasitism than eggs that did not induce the trait. In addition, Trichogramma wasps were attracted to volatiles of egg-induced plants that also expressed HR, and this attraction depended on the Trichogramma strain used. Consequently, HR did not have a negative effect on egg parasitoid survival. We conclude that even within a system where plants deploy lethal direct defences, such defences may still act with indirect defences in a synergistic manner to reduce herbivore pressure.     

Plant Quantity Affects Development and Survival of a Gregarious Insect Herbivore and Its Endoparasitoid Wasp

Virtually all studies of plant-herbivore-natural enemy interactions focus on plant quality as the major constraint on development and survival. However, for many gregarious feeding insect herbivores that feed on small or ephemeral plants, the quantity of resources is much more limiting, yet this area has received virtually no attention. Here, in both lab and semi-field experiments using tents containing variably sized clusters of food plants, we studied the effects of periodic food deprivation in a tri-trophic system where quantitative constraints are profoundly important on insect performance. The large cabbage white Pieris brassicae, is a specialist herbivore of relatively small wild brassicaceous plants that grow in variable densities, with black mustard (Brassica nigra) being one of the most important. Larvae of P. brassicae are in turn attacked by a specialist endoparasitoid wasp, Cotesia glomerata. Increasing the length of food deprivation of newly molted final instar caterpillars significantly decreased herbivore and parasitoid survival and biomass, but shortened their development time. Moreover, the ability of caterpillars to recover when provided with food again was correlated with the length of the food deprivation period. In outdoor tents with natural vegetation, we created conditions similar to those faced by P. brassicae in nature by manipulating plant density. Low densities of B. nigra lead to potential starvation of P. brassicae broods and their parasitoids, replicating nutritional conditions of the lab experiments. The ability of both unparasitized and parasitized caterpillars to find corner plants was similar but decreased with central plant density. Survival of both the herbivore and parasitoid increased with plant density and was higher for unparasitized than for parasitized caterpillars. Our results, in comparison with previous studies, reveal that quantitative constraints are far more important that qualitative constraints on the performance of gregarious insect herbivores and their gregarious parasitoids in nature.