Observations on the Ecology of Weaver Ants (Oecophylla smaragdina Fabricius) in a Thai Mangrove Ecosystem and Their Effect on Herbivory of Rhizophora mucronata Lam.

Ants of the genus Oecophylla are predators of other insects and are able to protect a variety of terrestrial plants against pest insects; however, observations on the ecology of these ants in mangrove forests are lacking. General observations on the ecology of Oecophylla smaragdina were carried out in a Thai mangrove forest to determine if these ants can protect their host plants in less favorable mangrove habitats. Leaf herbivory and the density of O. smaragdina ants were measured on Rhizophora mucronata trees at two sites. The results showed a negative correlation between ant density and herbivory. At both sites, the mean percent damaged leaf area was more than four times higher on trees without ants compared to “ant‐trees.” A significant negative correlation was found between tree mean percent leaf damage and the density of ants on the tree. Furthermore, on trees with ants, there was less herbivory on leaves close to ant nests compared to other leaves on the tree. Most damage was caused by chrysomelid beetles (62%) and sesarmid crabs (25%) and both types of herbivory were significantly reduced on ant‐trees.     

Effect of habitat complexity on biological control by the red imported fire ant (Hymenoptera: Formicidae) in collards

A potentially important and understudied biological control agent in US agroecosystems is the red imported fire ant, Solenopsis invicta Buren. Red imported fire ants may be particularly important biological control agents because we can manipulate their abundance with changes in habitat complexity. The effect of habitat complexity on biological control by fire ants was determined using plots of collards intercropped with white clover (complex habitat) and simple collard monocrops. The most economically significant pests of collards are larvae of the diamondback moth (DBM), Plutella xylostella (L.). Predation of DBM larvae by fire ants was more rapid and efficient in the intercrop than the monocrop. Red imported fire ants were 23% less abundant in the intercrop than the monocrop, however, suggesting that fire ants had a greater per capita effect on DBM survival in the complex habitat. Red imported fire ant predation of DBM larvae was significantly affected by larval density. Red imported fire ants also reduced the survival of leaf beetles, another economically significant pest taxa, by 45%. Furthermore, collard leaf damage tended to be inversely related to fire ant density and fire ants were more effective at reducing crop damage in the complex intercrop. Our study indicates the ability of red imported fire ants to be effective biological control agents and suggests that increasing habitat complexity can enhance red imported fire ant efficacy and herbivore control.     

Positive and negative effects of leaf shelters on herbivorous insects: linking multiple herbivore species on a willow

We experimentally examined the effects on other herbivorous insects of leaf shelters constructed by lepidopteran larvae on a willow, Salix miyabeana. Several insect species occupied the vacant leaf shelters. Our experiment using artificial leaf shelters showed that the number of aphids increased with the number of artificial leaf shelters on a shoot, as did the numbers of three ant species ( Camponotus japonicus, Lasius hayashi, and Myrmica jessensis) that entered leaf shelters to collect aphid honeydew. To determine the ant-mediated effect of leaf shelters on herbivorous insects that do not use leaf shelters, we transferred newly hatched larvae of a common leaf beetle, Plagiodera versicolora, to the leaves of shoots with and without artificial leaf shelters. One day after the transfer, larval survival rate was significantly lower on shoots with shelters than on those without shelters, and shoots with shelters had significantly more ants than did shoots without shelters. Our field experiments demonstrated clearly that shelter-making lepidopteran larvae increased the abundance of both aphids and ants and decreased the survival rate of leaf beetle larvae, probably because the larvae were removed by ants that were attracted to the leaf shelters by the aphid colonies.     

Biocontrol of <Emphasis Type="Italic">Cameraria ohridella</Emphasis> by insectivorous birds in different landscape contexts

The horse chestnut leaf miner (HCLM) Cameraria ohridella Deschka and Dimic (Lepidoptera, Gracillariidae) is a novel but significant pest in Europe. Current control measures are either inefficient or environmentally harmful. Tits (Parus spp.) open the mines and prey on HCLM, but the biocontrol efficiency of this behaviour has not yet been quantified. We installed bird nesting-boxes in a biennial field study on four sites close to Brunswick (Germany). On the same sites, we counted HCLM pupae, larvae, opened and closed mines, and parasitised larvae and pupae in leaves collected from horse chestnut (Aesculus hippocastanum L., Hippocastanaceae) trees with and without bird exclusion. In both years, the HCLM number and the proportion of closed mines were higher in bird exclusion trees, particularly on sites with high abundance of tits. Hence, we suggest including the facilitation of birds, particularly tits, in future HCLM biocontrol strategies.     

Genetic basis of resistance to fall armyworm (Lepidoptera: Noctuidae) and southwestern corn borer (Lepidoptera: Crambidae) leaf-feeding damage in maize

Leaf-feeding damage by first generation larvae of fall armyworm, Spodopter frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), and southwestern corn borer, Diatraea grandiosella Dyar (Lepidoptera: Crambidae), cause major economic losses each year in maize, Zea mays L. A previous study identified quantitative trait loci (QTL) contributing to reduced leaf-feeding damage by these insects in the maize line Mp704. This study was initiated to identify QTL and their interactions associated with first generation leaf-feeding damage by fall armyworm and southwestern corn borer. QTL associated with fall armyworm and southwestern corn borer resistance in resistant line Mp708 were identified and compared with Mp704. Multiple trait analysis (MTA) of both data sets was then used to identify the most important genetic regions affecting resistance to fall armyworm and southwestern corn borer leaf-feeding damage. Genetic models containing four and seven QTL explained southwestern corn borer and fall armyworm resistance, respectively, in Mp708. Key genomic regions on chromosomes 1, 5, 7, and 9 were identified by MTA in Mp704 and Mp708 that confer resistance to both fall armyworm and southwestern corn borer. QTL regions on chromosomes 1, 5, 7, and 9 contained resistance to both insects and were present in both resistant lines. These regions correspond with previously identified QTL related to resistance to other lepidopteran insects, suggesting that broad-spectrum resistance to leaf feeding is primarily controlled by only a few genetic regions in this germplasm.     

Wound-induced changes in tomato leaves and their effects on the feeding patterns of larval lepidoptera

Several studies have shown changes in the patterns of damage from feeding insects associated with changes in palatability and overall consumption as a result of wound-induced chemical changes in plants. This paper describes how the pattern of feeding damage made by the larvae of Spodoptera littoralis Boisd. (Lepidoptera: Noctuidae) on tomato is affected by changes in palatability of the leaves. Two sorts of responses to leaves from plants that had received prior damage were observed. Larvae offered a choice of leaves tended to take fewer meals on leaves from previously-wounded plants than on control leaves, frequently rejecting the former after sampling them. On wounded plants this rejection behaviour was associated with a shift in feeding site towards the base of the plant. However, starved larvae offered only a single excised leaf readily ate leaves from wounded plants but took shorter meals on these leaves than on controls. Although it was not directly tested it is possible that this difference in response reflected changes in food selectivity with a differing level of satiation. The results are considered in relation to the adaptive significance of the plant of changes in within-plant distributions of herbivore damage.     

Benefits conferred by “timid” ants: active anti-herbivore protection of the rainforest tree Leonardoxa africana by the minute ant Petalomyrmex phylax

In this study, we demonstrate that an important benefit provided by the small host-specific ant Petalomyrmex phylax to its host plant Leonardoxa africana is efficient protection against herbivores. We estimate that in the absence of ants, insect herbivory would reduce the leaf area by about one-third. This contributes considerably to the fitness of the plant. Our estimates take into account not only direct damage, such as removal of leaf surface by chewing insects, but also the effects of sucking insects on leaf growth and expansion. Sucking insects are numerically predominant in this system, and the hitherto cryptic effects of ant protection against the growth-reducing effects of sucking insects accounted for half of the total estimated benefit of ant protection. We propose that the small size of workers confers a distinct advantage in this system. Assuming that resource limitation implies a trade off between size and number of ants, and given the small size of phytophagous insects that attack Leonardoxa, we conclude that fine-grained patrolling by a large number of small workers maximises protection of young leaves of this plant. Since herbivores are small and must complete their development on the young leaves of Leonardoxa, and since a high patrolling density is required for a fine-grained search for these enemies, numerous small ants should provide the most effective protection of young leaves of Leonardoxa. We also discuss other factors that may have influenced worker size in this ant. Received: 1 September 1996 / Accepted: 2 June 1997     

Bird predation on herbivorous insects: indirect effects on sugar maple saplings

Insectivorous birds have been shown to have direct effects on abundances of herbivorous arthropods, but few studies have tested the indirect effects of birds on plant performance through consumption of herbivorous insects. In a 3-year study at the Hubbard Brook Experimental Forest, New Hampshire, we tested whether bird predation indirectly affects leaf herbivory levels and leaf and shoot biomass production of understory sugar maple (Acer saccharum) saplings. Trees were randomly assigned to one of four treatments: an insecticide application to reduce herbivory levels, exclosures that prevented bird access, addition of Lepidoptera larvae, and controls. Trees sprayed with an insecticide supported significantly fewer Lepidoptera larvae than other treatments throughout the study. Also, trees in exclosures supported more Lepidoptera larvae than controls during one count each year, and pooled across all counts during the second year. As predicted, the mean proportion of leaf area consumed varied significantly among treatments and was least in the insecticide treatment, followed by controls, exclosures, and Lepidoptera additions. Significant differences among treatments in herbivory levels, however, did not lead to differences in leaf or shoot biomass production. Thus, bird predation decreased Lepidoptera abundances and decreased herbivory levels, but did not increase biomass production during the following year. Over 85% of the herbivores in our study were Homoptera nymphs that were not folivorous and are not important bird prey items, potentially dampening the indirect effects of bird predation on biomass production. A comparison of these results with previous studies suggests that the indirect effects of bird predation on plant biomass production may depend on the plant species, abundance and composition of the herbivore community, and primary productivity of the ecosystem.     

Effects of Bt maize expressing Cry1Ab and Bt spray on Spodoptera littoralis

Various studies have been conducted to assess the damage caused by secondary lepidopteran pests to transgenic Bt maize expressing Cry1Ab. However, to date little is known on the effects of transgenic maize on Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae), a polyphagous herbivore which is considered a pest in Mediterranean maize growing areas. Here we present results on the effects of Bt maize (Bt‐11) and Bt spray (Dipel) on the various life stage parameters of this herbivore. We further assess the expression of Cry1Ab in different leaves and leaf parts in maize at a given plant growth stage, and determine whether the feeding damage of 3rd instar S. littoralis is influenced by Bt toxin expression. Contrary to previous literature reporting that S. littoralis is not sensitive to Bt Cry1Ab toxin, our results show that insects fed on either transgenic or Bt sprayed plants were negatively affected. Young S. littoralis larvae (1st and 2nd instars) were found to be the most sensitive to the Bt toxin. This was represented by a higher mortality and a slower developmental time of larvae maintained on transgenic or sprayed plants when compared to insects maintained on control plants. Moreover, Bt maize had a stronger and prolonged detrimental effect on insects when compared to Bt spray in maize. This was revealed by the fact that insects maintained on transgenic plants from 3rd instar to pupation took longer to reach adult emergence compared to insects that were maintained on sprayed plants. This was likely due to the continuous exposure of insects to the toxin when kept on transgenic maize. ELISA results showed a variation in the amount of Bt toxin among different leaf sections in transgenic maize at a given plant growth stage. These differences in Bt toxin were primarily found in the youngest leaf of growing plants. Although the lowest amounts of Bt toxin were detected in the growing leaf section of young leaves, this difference did not appear to influence the feeding behavior of 3rd instar S. littoralis.     

Plant-attracted ants affect arthropod community structure but not necessarily herbivory

Abstract.  1. The effectiveness of ants as plant defenders is equivocal for plants that attract ants via extrafloral nectaries (EFNs).
2. This study focused on the myrmecophilic savannah tree Pseudocedrela kotschyi that attracts ants to EFNs and on the arthropod fauna associated with P. kotschyi . Herbivory and arthropod community composition were compared between trees that were dominated by one of three congeneric ant species, Camponotus acvapimensis , C. rufoglaucus , and C. sericeus , and between trees where ants were experimentally excluded and untreated control trees.
3. Short-term ant-exclusion experiments failed to demonstrate a consistent effect of ants on herbivory.
4. Plants dominated by different ant species differed significantly in leaf damage caused by herbivorous insects. The relative ranking of herbivory levels of the trees dominated by different ant species was persistent in three consecutive years.
5. Ants significantly reduced the abundance of different arthropod groups (Araneae, Blattodea, Coleoptera, Homoptera, non-ant Hymenoptera). Other groups, including important herbivores, seemed not to be affected (Lepidoptera, Orthoptera, Thysanoptera, Heteroptera).
6. The study suggests that the presence of ants only benefits plants when specific ant species are attracted, and protection by these ants is not counterbalanced by their negative effect on other beneficial arthropods.     

Birds exploit herbivore‐induced plant volatiles to locate herbivorous prey

Arthropod herbivory induces plant volatiles that can be used by natural enemies of the herbivores to find their prey. This has been studied mainly for arthropods that prey upon or parasitise herbivorous arthropods but rarely for insectivorous birds, one of the main groups of predators of herbivorous insects such as lepidopteran larvae. Here, we show that great tits (Parus major) discriminate between caterpillar‐infested and uninfested trees. Birds were attracted to infested trees, even when they could not see the larvae or their feeding damage. We furthermore show that infested and uninfested trees differ in volatile emissions and visual characteristics. Finally, we show, for the first time, that birds smell which tree is infested with their prey based on differences in volatile profiles emitted by infested and uninfested trees. Volatiles emitted by plants in response to herbivory by lepidopteran larvae thus not only attract predatory insects but also vertebrate predators.     

Does ant predation favour leaf beetle specialization on toxic host plants?

Generalist predators are frequently seen as evolutionary forces that narrow the host range in herbivorous insects. Predators may favour specialization of herbivores on host plants containing toxic chemicals (which can be used by herbivores for their own defence) if host plant‐derived defences provide better protection from enemies than do autogenously produced defences. We compared the effectiveness of these two defensive strategies in the larvae of six species of leaf beetle (Chrysomelidae) against wood ants (Formica rufa group) in field experiments. Ants were more strongly repelled by larvae with host plant‐derived, salicylaldehyde‐containing secretions than by larvae with various autogenous secretions, but collectively foraging ants ultimately overcame any type of chemical defence by social interactions, chemical signalling, and olfactory learning. As a result, ants killed all larvae of Chrysomela lapponica defended by salicylaldehyde‐containing secretions within 2 days of their introduction to willows within 15 m of ant nests. We conclude that in the field neither type of chemical defence provides complete protection against wood ants in the vicinity of their nests, and that evolutionary shifts from autogenous production of secretion to sequestration of plant allelochemicals in leaf beetles may be favoured mostly at low ant densities on the periphery of ant foraging areas.     

Effects of aphids on foliar foraging by Argentine ants and the resulting effects on other arthropods

Abstract.  1. Although interactions between ants and honeydew-producing insects have received considerable study, relatively little is known about how these interactions alter the behaviour of ants in ways that affect other arthropods. In this study, field and greenhouse experiments were performed that examined how the presence of aphids ( Aphis fabae solanella ) on Solanum nigrum influenced the foraging behaviour of Argentine ants ( Linepithema humile ) and, in turn, modified the extent to which ants deter larval lacewings ( Chrysoperla rufilabris ), which are known aphid predators.
2. A field experiment demonstrated that the level of foliar foraging by ants increased linearly with aphid abundance, whereas no relationship existed between the level of ground foraging by ants and aphid abundance.
3. In the greenhouse, as in the field, foliar foraging by ants greatly increased when aphids were present. Higher levels of foliar foraging led to a twofold increase in the likelihood that ants contacted aphid predators. As a result of these increased encounters with ants, lacewing larvae were twice as likely to be removed from plants with aphids compared with plants without aphids. Once contact was made, however, the behaviour of ants towards lacewing larvae appeared similar between the two experimental groups.
4. Argentine ants drive away or prey upon a diversity of arthropod predators and parasitoids, but they also exhibit aggression towards certain herbivores. Future work should attempt to quantify how the ecological effects that result from interactions between honeydew-producing insects and invasive ants, such as L. humile , differ from those that result from interactions between honeydew-producing insects and native ants.     

Larval gregariousness and neonate establishment of the eucalypt-feeding beetle Chrysophtharta agricola (Coleoptera: Chrysomelidae: Paropsini)

The selective advantage offered to individuals living within groups may relate to natural enemy defence, but in leaf feeding insects may also relate to overcoming plant defences, especially with respect to feeding establishment. We conducted a series of experiments focusing on neonate larval survival, examining the effect of group size and leaf age on the survival of a eucalypt-feeding beetle, Chrysophtharta agricola , which formed groups of up to 43 larvae on the foliage of Eucalyptus nitens in the field. In the laboratory, in the absence of natural enemies, we found that initial density, leaf age and damage to the leaf margin significantly affected larval survival. Survival of solitary first-instar larvae on young foliage was around 80% whereas on older foliage it was around 11%. Prior damage to the leaf margin significantly increased survival on older leaves to around 61%. Initial larval density also affected survival, although mortality was always significantly higher on older leaves. On older leaves the larval group size above which mortality increased no further was over two-fold that on young leaves. Observations of group feeding behaviour at each instar showed that the majority of larvae (75.7%) were aligned facing away from the feeding site and that only around 7.5%, or just 1–2 larvae per group, fed at any one time. Feeding larvae chewed the leaf edge by straddling the leaf margin. Measurements of leaf margins showed that older leaves had significantly thicker leaf margins and 'thickness' ratios (leaf margin to leaf lamina proper). In the field, approximately 85% of all larvae occurred on the first two expanded leaf pairs, and larval mortality was highest between eclosion and establishment of the first instar. However, beetles apparently did not adjust clutch size according to leaf age.     

Damage to lima beans by Helicoverpa zea larvae treated as different instars with a nucleopolyhedrovirus

Larvae of the corn earworm,Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), were caged assecond, third, or fourth instars on lima bean,Phaseolus lunatus L., plants in the fieldwith or without treatment of the plants withlethal concentrations of the H. zeanucleopolyhedrovirus. The virus treatmentprevented over 90% of damage to pods and beansif larvae were second or third instars whenplaced in the cages. Damage to pods and beanswas reduced by 73 and 86%, respectively, ifthe larvae were fourth instars when placed onthe plants. When insects survived to the endof the test (which they did only on controlplants), numbers of pods or beans damaged byeach surviving insect was not affected by thestadium in which the larva was when it wasplaced on the plant. This result indicates thatmost damage was done by fourth or laterinstars. If treatments are to effectivelyprevent damage to lima bean, they should thusbe applied before the insects reach the fourthinstar.     

Within-tree variation in density and survival of leafminers on oak Quercus dentata

The density and survival of leafminers were examined on 50 sun leaves from each of 65 Quercus dentata Thunb. individuals in northern Japan in 1997 and 1998. Phyllonorycter (two species), Caloptilia (one species) and Stigmella (three species) were abundant or common on this oak in the study area. These leafminers appeared after mid-June, whereas most externally feeding caterpillars occurred from late May to early June when the water content and nitrogen concentration of leaves were high. The density of these leafminers was about four times higher in 1998 than in 1997. A negative correlation was more often observed between mine density and leaf size, leaf wet weight per area or leaf toughness in the Phyllonorycter species, but the opposite correlation was more frequent for Caloptilia and Stigmella species. Conversely, no clear relation was observed between the survival of Phyllonorycter larvae and leaf traits. In all leafminers except the gregarious Stigmella species, the mine density was more often positively correlated with leaf damage by chewing insects, and also the survival of Phyllonorycter larvae was often positively correlated with leaf damage. In the Phyllonorycter species, the survival of larvae tended to increase with the increase in density at the autumn generation. The correlation in the densities of mines between the summer and autumn generations was more frequently positive in the Phyllonorycter and Caloptilia species. In addition, the densities of different leafminers were often positively correlated. Thus, relations among leafminers, between leafminers and externally feeding caterpillars, and also between herbivores and host plants are complicated.     

Effects of neem oil on feeding behaviour and development of the pear sawfly, Caliroa cerasi

Neem oil deterred feeding by pear sawfly, Caliroa cerasi L., larvae (Hymenoptera: Tenthredinidae), both in choice and in no-choice cherry leaf disk bioassays. Deterrence was greater in the choice tests, with 50% inhibition occurring at 0.49% aqueous neem oil compared with 1.11% in the no-choice tests. Antifeedant activity towards pear sawfly larvae is slightly less than has been observed for Lepidoptera, but is higher than deterrence to other insects such as aphids. Topical application of neem oil to sawfly larvae resulted in reduced feeding, increased mortality, and a trend towards slower development. Most larval mortality after neem treatment resulted from incomplete subsequent moults. The potential utilization of neem insecticides for control of pear sawfly in tree fruit pest management is discussed.     

Experimental evaluation of the impacts of two ant species on banana weevil in Uganda

The banana weevil, Cosmopolites sordidus (Germar), is an important pest of bananas. Predatory ants are increasingly being viewed as possible biological control agents of this pest because they are capable of entering banana plants and soil in search of prey. We studied ant predation on banana weevil in Uganda in crop residues and live plants in both laboratory and field experiments. Field studies with live plants used chemical ant exclusion in some plots and ant enhancement via colony transfer in others to measure effects of Pheidole sp. 2 and Odontomachus troglodytes Santschi on plant damage and densities of immature banana weevils.In crop residues, an important pest breeding site, twice as many larvae were removed from ant-enhanced plots as in control plots. In young (2 month) potted suckers held in shade houses, ant ability to reduce densities of banana weevil life stages varied with the weevil inoculation rate. At the lowest density (2 female weevils per pot), densities of eggs, larvae, and pupae were reduced by ants. At higher rates there was no effect. In older suckers (5–11 months) grown in larger containers, banana weevil densities were not affected by ants, but damage levels were reduced. In a field trial lasting a full crop cycle (30 months), we found that the ants tested reduced the density of banana weevil eggs in suckers during the crop, but did not affect larval densities in the sampled suckers. However, most larvae occur in the main banana plants, rather than associated suckers. Nevertheless, levels of damage in mature plants at harvest did not differ between Amdro-treated and ant-enhanced plots, suggesting the ant species studied were not able to provide economic control of banana weevil under our test conditions.     

Expression of the peroxidase gene promoter (Shpx6b) from Stylosanthes humilis in transgenic plants during insect attack

Inducible promoters are important in regulating the expression of resistance genes when plants are attacked by insects or pathogens. Evaluation of the Shpx6b peroxidase promoter from the tropical forage legume Stylosanthes humilis[ Curtis MD, Rae AL, Rusu AG, Harrison SJ & Manners JM (1997) A peroxidase gene promoter induced by phytopathogens and methyl jasmonates in transgenic plants. Molecular Plant Microbial Interactions 10: 326–338] in transgenic tobacco plants Nicotiana tabacum L. (Solanaceae) demonstrated that this promoter could drive expression of both the β‐glucuronidase (GUS uidA gene of E. coli) and green fluorescent protein (GFP) reporter genes in leaf tissues during attack by chewing insects – larvae of potato tuber moth (PTM) Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae) and sucking insects – green peach aphids Myzus persicae Sulzer (Homoptera: Aphididae). Strong GUS expression was present in tissues next to cells damaged by PTM larvae 24 h after infestation. With aphid infestation, GUS expression was limited to sites of feeding, and was observed 48 h after infestation. The expression of GFP mirrored that of GUS expression for both treatments, but was normally detected 48 h after infestation. Similarly, the exogenous application of methyl jasmonate (MeJa) induced GUS uniformly across leaf tissue, and mechanical wounding activated GUS expression at wound sites, similar to PTM larvae. GFP expression was observed 48 h after treatment, and for mechanical wounding GFP was localised in a manner similar to PTM damage. For MeJa treatment, GFP expression was more pronounced in cells around the midrib, and it was not uniformly induced across the leaf tissue. GUS reporter gene levels were also assayed to quantify expression, and the results were consistent with the observed histological patterns of expression. The results presented here show that the Shpx6b promoter switches on the expression of linked genes after damage by insect herbivores, and could be useful in regulating the expression of heterologous genes for insect and/or pathogen resistance in transgenic plants.     

Coordinated group ambush: A new predatory behavior inAzteca ants (Dolichoderinae)

Summary This article describes a new technique used by ants (Azteca cf. lanuginosa) in the Brazilian Cerrado to capture large mobile insects. Large numbers of ants position themselves along a leaf margin in sit-and-wait groups and ambush prey by simultaneously attacking insects that land on the upper surface of the leaf. The workers are able to seize insects such as beetles, bees, and butterflies, most of them being two times longer than the ants.