Crop and landscape heterogeneity increase biodiversity in agricultural landscapes: A global review and meta-analysis.

Agricultural intensification not only increases food production but also drives widespread biodiversity decline. Increasing landscape heterogeneity has been suggested to increase biodiversity across habitats, while increasing crop heterogeneity may support biodiversity within agroecosystems. These spatial heterogeneity effects can be partitioned into compositional (land-cover type diversity) and configurational heterogeneity (land-cover type arrangement), measured either for the crop mosaic or across the landscape for both crops and semi-natural habitats. However, studies have reported mixed responses of biodiversity to increases in these heterogeneity components across taxa and contexts. Our meta-analysis covering 6397 fields across 122 studies conducted in Asia, Europe, North and South America reveals consistently positive effects of crop and landscape heterogeneity, as well as compositional and configurational heterogeneity for plant, invertebrate, vertebrate, pollinator and predator biodiversity. Vertebrates and plants benefit more from landscape heterogeneity, while invertebrates derive similar benefits from both crop and landscape heterogeneity. Pollinators benefit more from configurational heterogeneity, but predators favour compositional heterogeneity. These positive effects are consistent for invertebrates and vertebrates in both tropical/subtropical and temperate agroecosystems, and in annual and perennial cropping systems, and at small to large spatial scales. Our results suggest that promoting increased landscape heterogeneity by diversifying crops and semi-natural habitats, as suggested in the current UN Decade on Ecosystem Restoration, is key for restoring biodiversity in agricultural landscapes.

Insect pest damage increases faba bean (Vicia faba) yield components but only in the absence of insect pollination.

Identifying and quantifying crop stressors interactions in agroecosystems is necessary to guide sustainable crop management strategies. Over the last 50 years, faba bean cropping area has been declining, partly due to yield instabilities associated with uneven insect pollination and herbivory. Yet, the effect of interactions between pollinators and a key pest, the broad bean beetle Bruchus rufimanus (florivorous and seed predating herbivore) on faba bean yield has not been investigated. Using a factorial cage experiment in the field, we investigated how interactions between two hypothesized stressors, lack of insect pollination by bumblebees and herbivory by the broad bean beetle, affect faba bean yield. Lack of bumblebee pollination reduced bean weight per plant by 15%. Effects of the broad bean beetle differed between the individual plant and the plant-stand level (i.e., when averaging individual plant level responses at the cage level), likely due to high variation in the level of herbivory among individual plants. At the individual plant level, herbivory increased several yield components but only in the absence of pollinators, possibly due to plant overcompensation and/or pollination by the broad bean beetle. At the plant-stand level, we found no effect of the broad bean beetle on yield. However, there was a tendency for heavier individual bean weight with bumblebee pollination, but only in the absence of broad bean beetle herbivory, possibly due to a negative effect of the broad bean beetle on the proportion of legitimate flower visits by bumblebees. This is the first experimental evidence of interactive effects between bumblebees and the broad bean beetle on faba bean yield. Our preliminary findings of negative and indirect associations between the broad bean beetle and individual bean weight call for a better acknowledgment of these interactions in the field in order to understand drivers of crop yield variability in faba bean.

Water stress and insect herbivory interactively reduce crop yield while the insect pollination benefit is conserved.

Climate change is predicted to hamper crop production due to precipitation deficits and warmer temperatures inducing both water stress and increasing herbivory due to more abundant insect pests. Consequently, crop yields will be impacted simultaneously by abiotic and biotic stressors. Extensive yield losses due to such climate change stressors might, however, be mitigated by ecosystem services such as insect pollination. We examined the single and combined effects of water stress, insect herbivory and insect pollination on faba bean yield components and above- and belowground plant biomass under realistic field conditions. We used rainout shelters to simulate a scenario in line with climate change projections, with adequate water supply at sowing followed by a long period without precipitation. This induced a gradually increasing water stress, culminating around crop flowering and yield formation. We found that gradually increasing water stress combined with insect herbivory by aphids interactively shaped yield in faba beans. Individually, aphid herbivory reduced yield by 79% and water stress reduced yield by 52%. However, the combined effect of water stress and aphid herbivory reduced yield less (84%) than the sum of the individual stressor effects. In contrast, insect pollination increased yield by 68% independently of water availability and insect herbivory. Our results suggest that yield losses can be greatly reduced when both water stress and insect herbivory are reduced simultaneously. In contrast, reducing only one stressor has negligible benefits on yield as long as the crop is suffering from the other stressor. We call for further exploration of interactions among ecosystem services and biotic and abiotic stressors that simulate realistic conditions under climate change.

Head roll stabilisation in the nocturnal bull ant Myrmecia pyriformis: implications for visual navigation.

Ant foragers are known to memorise visual scenes that allow them to repeatedly travel along idiosyncratic routes and to return to specific places. Guidance is provided by a comparison between visual memories and current views, which critically depends on how well the attitude of the visual system is controlled. Here we show that nocturnal bull ants stabilise their head to varying degrees against locomotion-induced body roll movements, and this ability decreases as light levels fall. There are always un-compensated head roll oscillations that match the frequency of the stride cycle. Head roll stabilisation involves both visual and non-visual cues as ants compensate for body roll in complete darkness and also respond with head roll movements when confronted with visual pattern oscillations. We show that imperfect head roll control degrades navigation-relevant visual information and discuss ways in which navigating ants may deal with this problem.

Follower ants in a tandem pair are not always naïve.

In addition to foraging individually several species of ants guide nestmates to a goal by tandem running. We found that the Australian ant, Camponotus consobrinus, forages both individually and by tandem running to head to the same goal, nest-specific native Australian trees on which they forage. While paths of solitary foragers and initial paths of tandem followers showed no differences in heading directions or straightness, tandem followers moved at about half the speed of solitary runs. When leaders were experimentally removed, follower ants initially engaged in a systematic search around the point of interruption, following which they either (a) headed directly towards and successfully reached the foraging trees, or (b) continued searching or (c) returned to the nest. The high incidence of followers that successfully navigated towards the foraging trees on their own provides strong evidence that many tandem followers are in fact experienced foragers. Detailed analysis of the searching behaviour revealed that even seemingly lost followers displayed a directional bias towards the foraging trees in their search path. Our results show that in a foraging context follower ants in a tandem pair are not always naïve.

Compound eye adaptations for diurnal and nocturnal lifestyle in the intertidal ant, Polyrhachis sokolova.

The Australian intertidal ant, Polyrhachis sokolova lives in mudflat habitats and nests at the base of mangroves. They are solitary foraging ants that rely on visual cues. The ants are active during low tides at both day and night and thus experience a wide range of light intensities. We here ask the extent to which the compound eyes of P. sokolova reflect the fact that they operate during both day and night. The ants have typical apposition compound eyes with 596 ommatidia per eye and an interommatidial angle of 6.0°. We find the ants have developed large lenses (33 µm in diameter) and wide rhabdoms (5 µm in diameter) to make their eyes highly sensitive to low light conditions. To be active at bright light conditions, the ants have developed an extreme pupillary mechanism during which the primary pigment cells constrict the crystalline cone to form a narrow tract of 0.5 µm wide and 16 µm long. This pupillary mechanism protects the photoreceptors from bright light, making the eyes less sensitive during the day. The dorsal rim area of their compound eye has specialised photoreceptors that could aid in detecting the orientation of the pattern of polarised skylight, which would assist the animals to determine compass directions required while navigating between nest and food sources.

Homing abilities of the Australian intertidal ant Polyrhachis sokolova.

The pressure of returning to and locating the nest after a successful foraging trip is immense in ants. To find their way back home, ants use a number of different strategies (e.g. path integration, trail following) and rely on a range of cues (e.g. pattern of polarised skylight, landmark panorama) available in their environment. How ants weigh different cues has been a question of great interest and has primarily been addressed in the desert ants from Africa and Australia. We here identify the navigational abilities of an intertidal ant, Polyrhachis sokolova, that lives on mudflats where nests and foraging areas are frequently inundated with tidal water. We find that these solitary foraging ants rely heavily on visual landmark information for navigation, but they are also capable of path integration. By displacing ants with and without vector information at different locations within the local familiar territory, we created conflicts between information from the landmarks and information from the path integrator. The homing success of full-vector ants, compared with the zero-vector ants, when displaced 5 m behind the feeder, indicate that vector information had to be coupled with landmark information for successful homing. To explain the differences in the homing abilities of ants from different locations we determined the navigational information content at each release station and compared it with that available at the feeder location. We report here the interaction of multiple navigation strategies in the context of the information content in the environment.

Navigational efficiency of nocturnal Myrmecia ants suffers at low light levels.

Insects face the challenge of navigating to specific goals in both bright sun-lit and dim-lit environments. Both diurnal and nocturnal insects use quite similar navigation strategies. This is despite the signal-to-noise ratio of the navigational cues being poor at low light conditions. To better understand the evolution of nocturnal life, we investigated the navigational efficiency of a nocturnal ant, Myrmecia pyriformis, at different light levels. Workers of M. pyriformis leave the nest individually in a narrow light-window in the evening twilight to forage on nest-specific Eucalyptus trees. The majority of foragers return to the nest in the morning twilight, while few attempt to return to the nest throughout the night. We found that as light levels dropped, ants paused for longer, walked more slowly, the success in finding the nest reduced and their paths became less straight. We found that in both bright and dark conditions ants relied predominantly on visual landmark information for navigation and that landmark guidance became less reliable at low light conditions. It is perhaps due to the poor navigational efficiency at low light levels that the majority of foragers restrict navigational tasks to the twilight periods, where sufficient navigational information is still available.

Flicker is part of a multi-cue response criterion in fiddler crab predator avoidance.

Predator avoidance behaviour costs time, energy and opportunities, and prey animals need to balance these costs with the risk of predation. The decisions necessary to strike this balance are often based on information that is inherently imperfect and incomplete because of the limited sensory capabilities of prey animals. Our knowledge, however, about how prey animals solve the challenging task of restricting their responses to the most dangerous stimuli in their environment is very limited. Using dummy predators, we examined the contribution of visual flicker to the predator avoidance response of the fiddler crab Uca vomeris. The results illustrate that crabs let purely black or purely white dummies approach significantly closer than black-and-white flickering dummies. We show that this effect complements other factors that modulate escape timing such as retinal speed and the crab's distance to its burrow, and is therefore not due exclusively to an earlier detection of the flickering signal. By combining and adjusting a range of imperfect response criteria in a way that relates to actual threats in their natural environment, prey animals may be able to measure risk and adjust their responses more efficiently, even under difficult or noisy sensory conditions.

Habituation under natural conditions: model predators are distinguished by approach direction.

Habituation is an active process that allows animals to learn to identify repeated, harmless events, and so could help individuals deal with the trade-off between reducing the risk of predation and minimizing escape costs. Safe habituation requires an accurate distinction between dangerous and harmless events, but in natural environments such an assessment is challenging because sensory information is often noisy and limited. What, then, comprises the information animals use to recognize objects that they have previously learned to be harmless? We tested whether the fiddler crab Uca vomeris distinguishes objects purely by their sensory signature or whether identification also involves more complex attributes such as the direction from which an object approaches. We found that crabs habituated their escape responses after repeated presentations of a dummy predator consistently approaching from the same compass direction. Females habituated both movement towards the burrow and descent into the burrow, whereas males only habituated descent into the burrow. The crabs were more likely to respond again when a physically identical dummy approached them from a new compass direction. The crabs distinguished between the two dummies even though both dummies were visible for the entire duration of the experiment and there was no difference in the timing of the dummies' movements. Thus, the position or approach direction of a dummy encodes important information that allows animals to identify an event and habituate to it. These results argue against the traditional notion that habituation is a simple, non-associative learning process, and instead suggest that habituation is very selective and uses information to distinguish between objects that is not available from the sensory signature of the object itself.