Unraveling navigational strategies in migratory insects

Long-distance migration is a strategy some animals use to survive a seasonally changing environment. To reach favorable grounds, migratory animals have evolved sophisticated navigational mechanisms that rely on a map and compasses. In migratory insects, the existence of a map sense (sense of position) remains poorly understood, but recent work has provided new insights into the mechanisms some compasses use for maintaining a constant bearing during long-distance navigation. The best-studied directional strategy relies on a time-compensated sun compass, used by diurnal insects, for which neural circuits have begun to be delineated. Yet, a growing body of evidence suggests that migratory insects may also rely on other compasses that use night sky cues or the Earth's magnetic field. Those mechanisms are ripe for exploration.     

Avian navigation and geographic positioning

Site fidelity to breeding and wintering grounds, and even stopover sites, suggests that passerines are capable of accurate navigation during their annual migrations. Geolocator‐based studies are beginning to demonstrate precise population‐specific migratory routes and even some interannual consistency in individual routes. Displacement studies of birds have shown that at least adult birds are capable of goal‐oriented movements, likely involving some type of map or geographic position system. In contrast, juveniles on their first migration use a clock‐and‐compass orientation strategy, with limited knowledge about locations along their migratory routes. Positioning information could come from a variety of cues including visual, olfactory, acoustic, and geomagnetic sources. How information from these systems is integrated and used for avian navigation has yet to be fully articulated. In this review, we (1) define geographic positioning and distinguish the types of navigational strategies that birds could use for orientation, (2) describe sensory cues available to birds for geographic positioning, (3) review the evidence for geographic positioning in birds and methods used to collect that evidence, and (4) discuss ways ornithologists, particularly field ornithologists, can contribute to and advance our knowledge of the navigational abilities of birds. Few studies of avian orientation and navigation mechanisms have been conducted in the Western Hemisphere. To fully understand migratory systems in the Western Hemisphere and develop better conservation policies, information about the orientation and navigation mechanisms used by specific species needs to be integrated with other aspects of their migration ecology and biology.     

What is geometric information and how do animals use it?

Unlike investigations of animals’ use of spatial cues such as landmarks, studies of sensitivity to the geometry of surfaces in an enclosure have proceeded mostly as an attempt to explain a laboratory finding with few direct tests of how animals use such a cue in nature. In this brief review, I discuss the current debate over whether global or local information from the enclosure drives the typical rotational error pattern in such studies. A consideration of the form and function of geometric cues in natural settings suggests that the natural boundaries for which arena walls are considered analogous might better be thought as landmarks. With a clearer picture of what geometric information is and how it might be used in nature, the generality of findings from laboratory studies of geometry enclosure can be better assessed.     

Effects of burrow condition and seed handling time on hoarding strategies of Edward's long-tailed rat (Leopoldamys edwardsi)

Many hoarding rodents use burrows not only for dwelling and protection from natural enemies, but also for food storage. However, little is known how burrows used by scatter-hoarding animals influence their foraging behaviors. In addition, handling time for a given food item has a fundamental impact on hoarding strategies of these hoarding animals: food items with longer handling time are more likely to be hoarded due to increasing predation risk because the animals spend more time outside their burrows if they consumed such food. By providing with two types of artificial burrows (aboveground vs. underground) and two types of food items (i.e. seeds) with contrasting handling times, we investigated how burrow condition and handling time co-influence hoarding strategies of a key scatter-hoarding rodent, Edward's long-tailed rat (Leopoldamys edwardsi) in large enclosures in southwest China. We found that only a few animals larder-hoarded fewer seeds when only aboveground burrows were available, while over 80% of the animals preferred to use the underground burrows and hoard significantly more seeds in the burrows when both aboveground and underground burrows were provided simultaneously. We also found that seed handling time significantly affected hoarding strategies of the animals: they consumed and/or scatter-hoarded more Camellia oleifera seeds with shorter handling time outside the burrow, but consumed and larder-hoarded more Lithocarpus harlandii seeds with longer handling time in underground burrows. Our study indicates that both burrow types and seed handling time have important impacts on hoarding strategies of scatter-hoarding animals.     

Directed vertebrate-mediated seed dispersal of a fleshy-fruited amaryllid in a heterogenous habitat

Most plants with fleshy fruits have seeds that are ingested by animals, but a less well-understood mode of seed dispersal involves fleshy fruits containing seeds that are discarded by frugivorous animals because they are too large or toxic to be ingested. We studied the seed dispersal biology of Haemanthus deformis, an amaryllid lily species found in a mosaic of bush clumps in a grassland matrix in South Africa. We asked whether seed dispersal is directed in and among bush clumps and whether germination and survival are greater for seeds dispersed to bush clumps than for those dispersed into grassland. Using camera trapping, we found that fruits are consumed mainly by birds and rodents. The pulp was removed from the seeds which were then discarded without ingestion. While many seeds were dispersed close to the parent plant, most (c. 78.5%) were dispersed further than 1 m away from the parent plant. Longer distance dispersal resulted mainly from birds flying off with fruits in their bill or from rodents engaging in scatter-hoarding behavior. Seedling survival was most successful within bush clumps as compared to grasslands and shade was identified as a primary requirement for seedling survival. Seeds from which the fruit pulp had been removed germinated faster than those in intact fruits. Haemanthus deformis deploys a system of directed seed dispersal, whereby both birds and rodents contribute to the dispersal of seeds within patchy bush clumps that are favorable for seedling survival.     

动物分散贮食行为对植物种群更新的影响

分散贮食是许多动物取食行为策略的重要组成部分。对以植物种子为主要贮食对象的动物来说,种子内营养物质含量、种子大小以及种子内次生化合物的含量等因素都直接影响动物的贮食行为。动物偏爱贮藏个体较大的种子,大种子多被搬运并分散贮藏在远离种源的地方,而小种子则多被就地取食,以补充动物贮食过程中的能量消耗。贮食动物主要通过空间记忆、特殊路线以及贮藏点周围的直接线索等途径重新获取贮藏点内食物。在重取过程中,一些贮藏点被遗忘,其中的种子成为植物种群更新的潜在种子库。因此,分散贮食动物不仅是种子捕食者,还是种子传播者,它们对植物种子的捕食、搬运和贮藏,影响了植物种子的存活和幼苗的建成,从而在一定程度上影响植物种群的更新、分布。植物种群为了促进种子的传播,在进化过程中逐渐形成了形式多样的适应性策略,降低种子的直接被捕食率,提高种子的被贮藏率。研究动物分散贮食行为对植物种群更新的影响,将有助于理解贮食动物与植物之间的互惠关系,从而认识贮食动物种群在生态系统中的作用,为生物多样性的保护提供科学依据。     

A red knot as a black swan: how a single bird shows navigational abilities during repeat crossings of the Greenland Icecap

Despite the wealth of studies on seasonal movements of birds between southern nonbreeding locations and High Arctic breeding locations, the key mechanisms of navigation during these migrations remain elusive. A flight along the shortest possible route between pairs of points on a sphere (‘orthodrome’) requires a bird to be able to assess its current location in relation to its migration goal and to make continuous adjustment of heading to reach that goal. Alternatively, birds may navigate along a vector with a fixed orientation (‘loxodrome’) based on magnetic and/or celestial compass mechanisms. Compass navigation is considered especially challenging for summer migrations in Polar regions, as continuous daylight and complexity in the geomagnetic field may complicate the use of both celestial and magnetic compasses here. We examine the possible use of orientation mechanisms during migratory flights across the Greenland Icecap. Using a novel 2 g solar-powered satellite transmitter, we documented the flight paths travelled by a female red knot Calidris canutus islandica during two northward and two southward migrations. The geometry of the paths suggests that red knots can migrate across the Greenland Icecap along the shortest-, orthodrome-like, path instead of the previously suggested loxodrome path. This particular bird's ability to return to locations visited in a previous year, together with its sudden course changes (which would be appropriate responses to ambient wind fields), suggest a map sense that enables red knots to determine location, so that they can tailor their route depending on local conditions.     

Does acoustically simulated predation risk affect settlement and reproduction of a migratory passerine?

Nest predation is one of the most important drivers of avian life history evolution and population dynamics. Increasing evidence suggests that birds are able to assess nest predation risk and avoid settling in high‐risk areas to increase their reproductive performance. However, the cues used for settlement decisions are poorly known in most species. Population sizes of the migratory wood warbler Phylloscopus sibilatrix are characterized by strong annual fluctuations, which are negatively correlated with the number of forest rodents. Wood warblers might avoid rodent‐rich areas to reduce predation risk arising either from rodents, from rodent‐hunting predators attracted to such areas or from predators not linked to rodents. To evaluate these hypotheses, we conducted a large‐scale field experiment to test whether wood warblers avoided settling in plots with high predation risk simulated by broadcasting vocalizations of rodents or predators. Moreover, we tested whether reproductive performance varied in relation to simulated predation risk. Settlement patterns did not differ between plots with rodent, predator and noise control treatments. Likewise, measures of reproductive performance did not seem to differ across treatments. Thus, the broadcasted vocalizations of rodents and predators did not seem to be perceived as threat by wood warblers. Alternatively, the species might use other cues than those presented here, either other acoustic cues, visual and/or olfactory cues or a combination of cue types during settlement. Further experimental investigations to pin point cues and senses relevant for settlement decisions in wood warblers and birds in general are needed to better understand their life history and population dynamics.     

Teasing Apart the Effects of Seed Size and Energy Content on Rodent Scatter-Hoarding Behavior

Scatter-hoarding rodents are known to play a crucial role in the seed dispersal of many plant species. Numerous studies have indicated that both seed size and the energy content of seeds can affect rodent foraging behavior. However, seed size is usually associated with energy content per seed, making it difficult to isolate how seed size and energy affect rodent foraging preferences. This study used 99 treatments of artificial seeds (11 seed sizes×9 levels of energy content) to tease apart the effect of seed size and energy content on rodent seed-caching behavior. Both seed traits showed significant effects, but their details depended on the stage of the rodent foraging process. Seeds with higher energy content were harvested more rapidly while seed size only had a modest effect on harvest rate. However, after harvesting, seed size showed a much stronger effect on rodent foraging behavior. Rodents’ choice of which seeds to remove and cache, as well as seed dispersal distance, seemed to reflect an optimal seed size. Our findings could be adapted in future studies to gain a better understanding of scatter-hoarding rodent foraging behavior, and the co-evolutionary dynamics between plant seed production and seed dispersers.     

Encoding new episodes and making them stick

How do we encode, store, and retrieve new episodic memories, and what are the computations performed by the hippocampus during this process? One system that has been used to model the brain basis of episodic memory in humans is the study of spatial navigation by path integration in rodents. Here I discuss three exciting new findings focused on encoding or replay of spatial sequences in the rat hippocampus. These findings not only provide important new insight into the computations associated with encoding and consolidation of spatial trajectories, but may also have implications for understanding key aspects of human episodic memory.     

Rats’ use of geometric, featural and orientation cues to locate a hidden goal

Over the past 20 years, a great deal of research has examined how different animals can use the geometric properties of the environment to determine their heading. Less well studied is how rats use the geometric properties of an environment to navigate, or determine the location, when it is not necessary to establish heading. Specifically, it is unclear to what extent rats still rely on geometric cues when they are not disoriented. In the current study, rats were trained to find food in one corner of a rectangular environment under either oriented or disoriented conditions. Probe tests placed geometric, featural and orientation cues in conflict. Results showed that featural cues exerted little control over the rats’ search preferences. All rats, whether trained while oriented or trained while disoriented, used geometric cues when these were the only cues available. Rats trained in the disoriented condition preferred geometric cues to orientation cues, whereas rats trained in the oriented condition showed more equal preference for orientation and geometric cues.     

Ultraviolet vision and foraging in terrestrial vertebrates

Tetrachromatic colour vision, based on four ‘main’ colours and their combinations, is probably the original colour vision in terrestrial vertebrates. In addition to human visible waveband of light (400–700 nm) and three main colours, it also includes the near ultraviolet part of light spectrum (320–400 nm). The ecological importance of ultraviolet (UV) vision in animals has mainly been studied in the context of intra‐ and inter‐sexual signalling, but recently the importance of UV vision in foraging has received more attention. Foraging animals may use either UV cues (reflectance or absorbance) of food items or UV cues of the environment. So far, all diurnal birds studied (at least 35 species), some rodents (4 species), many reptilians (11 species) and amphibians (2 species) are likely able to see near UV light. This probably allows e.g. diurnal raptors as well as frugivorous, nectarivorous and insectivorous birds to use foraging cues invisible to humans. The possible role of UV cues and existing light conditions should be taken into account when food selection of vertebrate animals is studied, particularly, in experiments with artificial food items.     

啮齿动物的分散贮食行为

食物贮藏是许多动物重要的适应性行为,分散贮藏的食物以植物种子为主。每个贮藏点贮藏数量不等的食物项目。啮齿动物分散贮藏食物之后,可降低食物被其他个体获取的机率,提高对食物资源的控制能力,最终有利于自身的生存和繁殖成功。植物种子被贮藏之后,可减少非贮食鼠类对种子的取食。同时,合适的微生境和埋藏有利于种子萌发、幼苗建成和植物的更新;使植物的分布区得以扩展。探讨啮齿动物的分散贮食行为,能够更好地理解食物贮藏在啮齿动物生活史中的作用,进一步认识鼠类和植物的相互关系以及不同啮齿动物在群落形成中的潜在作用。本综述了啮齿动物分散贮食的研究进展,并提出今后工作中的几点建议。     

A Comparison of Frugivory and Scatter-Hoarding Seed-Dispersal Syndromes

Frugivory (animals ingest all or part of fleshy-fruits and defecate or regurgitate seeds) and scatter-hoarding (animals store seeds in small caches in soil) are two important vertebrate-mediated seed dispersal syndromes. In both instances, there is an exchange of food for seed transport, but there are many important differences. For example, the seeds of frugivore-dispersed plants are often clumped in feces or under roosts and the microsite of depostion is often unsuitable for seedling establishment. However, frugivores can transport seeds long distances allowing plants to colonize new areas and promoting gene flow between populations. Scatter-hoarding animals, on the other hand, actively space seeds in microsites that often favor seedling establishment, but don’t move seeds very far. Both modes of seed dispersal can be very effective, but in different way. Some species of plants have evolved propagules that take advantage of both modes of dispersal in two separate phases (i.e., diplochory), apparently to obtain both types of benefits.     

The Modulation by Intensity of the Processing of Interaural Timing Cues for Localizing Sounds

Features of sounds such as time and intensity are important binaural cues for localizing their sources. Interaural time differences (ITDs) and interaural level differences are extracted and processed in parallel by separate pathways in the brainstem auditory nuclei. ITD cues are small, particularly in small-headed animals, and processing of these cues is optimized by both morphological and physiological specializations. Moreover, recent observations in mammals and in some birds indicate that interaural time and level cues are not processed independently but cooperatively to improve the detection of interaural differences. This review will specifically summarize what is known about how inhibitory circuits improve the measurements of ITD in a sound-level-dependent manner.     

Diplochory in western chokecherry: you can��t judge a fruit by its mesocarp

Western chokecherry (Prunus virginiana var. demissa, Rosaceae) is dispersed by frugivorous birds and carnivores, but it has large seeds that are potentially attractive to rodents that could act as seed predators and dispersers. Here, we quantify the benefits of primary dispersal by birds and secondary dispersal by scatter-hoarding rodents. In the fall, avian frugivores (mostly American robins, Turdus migratorius, and cedar waxwings, Bombycilla cedrorum) consumed 87% of the fruit crop and dispersed 67% of the fruit crop away from parent plants. Rodents removed 89% of seeds that simulated bird-dispersed seed rain from transects in riparian zones and 58% from transects in upland habitats. Rodents scatter-hoarded 91.6% of the seeds they removed, burying most in small caches (two to eight seeds) 8?C25?mm deep. About 39% of the seeds in spring caches produced seedlings. Inside rodent-proof exclosures, 52.1% of seeds buried to simulate rodent caches produced seedlings, 29.7% of which were still alive after 1?year. In contrast, only 3.8% of seeds placed on the soil surface, simulating dispersal by avian frugivores, produced seedlings. Seed dispersal by frugivorous birds likely contributes to colonization of unoccupied habitat through long-range dispersal and to escape from distance-dependent seed mortality near the parent plant. Despite seed losses, rodents offer short-range seed dispersal and bury seeds in more favorable sites for germination, improving seedling emergence and establishment. The combined mechanisms of seed dispersal significantly enhanced chokecherry seedling recruitment by providing more dispersal-related benefits than either frugivorous bird or scatter-hoarding rodents could provide alone.     

Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus

A well-developed spatial memory is important for many animals, but appears especially important for scatter-hoarding species. Consequently, the scatter-hoarding system provides an excellent paradigm in which to study the integrative aspects of memory use within an ecological and evolutionary framework. One of the main tenets of this paradigm is that selection for enhanced spatial memory for cache locations should specialize the brain areas involved in memory. One such brain area is the hippocampus (Hp). Many studies have examined this adaptive specialization hypothesis, typically relating spatial memory to Hp volume. However, it is unclear how the volume of the Hp is related to its function for spatial memory. Thus, the goal of this article is to evaluate volume as a main measurement of the degree of morphological and physiological adaptation of the Hp as it relates to memory. We will briefly review the evidence for the specialization of memory in food-hoarding animals and discuss the philosophy behind volume as the main currency. We will then examine the problems associated with this approach, attempting to understand the advantages and limitations of using volume and discuss alternatives that might yield more specific hypotheses. Overall, there is strong evidence that the Hp is involved in the specialization of spatial memory in scatter-hoarding animals. However, volume may be only a coarse proxy for more relevant and subtle changes in the structure of the brain underlying changes in behaviour. To better understand the nature of this brain/memory relationship, we suggest focusing on more specific and relevant features of the Hp, such as the number or size of neurons, variation in connectivity depending on dendritic and axonal arborization and the number of synapses. These should generate more specific hypotheses derived from a solid theoretical background and should provide a better understanding of both neural mechanisms of memory and their evolution.     

Neurally Encoding Time for Olfactory Navigation

Accurately encoding time is one of the fundamental challenges faced by the nervous system in mediating behavior. We recently reported that some animals have a specialized population of rhythmically active neurons in their olfactory organs with the potential to peripherally encode temporal information about odor encounters. If these neurons do indeed encode the timing of odor arrivals, it should be possible to demonstrate that this capacity has some functional significance. Here we show how this sensory input can profoundly influence an animal’s ability to locate the source of odor cues in realistic turbulent environments—a common task faced by species that rely on olfactory cues for navigation. Using detailed data from a turbulent plume created in the laboratory, we reconstruct the spatiotemporal behavior of a real odor field. We use recurrence theory to show that information about position relative to the source of the odor plume is embedded in the timing between odor pulses. Then, using a parameterized computational model, we show how an animal can use populations of rhythmically active neurons to capture and encode this temporal information in real time, and use it to efficiently navigate to an odor source. Our results demonstrate that the capacity to accurately encode temporal information about sensory cues may be crucial for efficient olfactory navigation. More generally, our results suggest a mechanism for extracting and encoding temporal information from the sensory environment that could have broad utility for neural information processing.     

Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning

BACKGROUND: Associative memory formation requires that animals choose predictors for experiences they need to remember. When an artificial odor is paired with an aversive experience, that odor becomes the predictor. In more natural settings, however, animals can have multiple salient experiences that need to be remembered and prioritized. The mechanisms by which animals deal with multiple experiences are incompletely understood. RESULTS: Here we show that Drosophila males can be trained to discriminate between different types of female pheromones; they suppress courtship specifically to the type of female that was associated with unsuccessful courtship. Such "trainer-specific" learning is mediated by hydrocarbon olfactory cues and modifies the male's processing of those cues. Animals that are unable to use olfactory cues can still learn by using other sensory modalities, but memory in this case is not specific to the trainer female's maturation state. Concurrent and serial presentation of different pheromones demonstrates that the ability to consolidate memory of pheromonal cues can be modified by the temporal order in which they appear. CONCLUSION: Suppression of memory by new learning demonstrates that the dynamics of memory consolidation are subject to plasticity in Drosophila. This type of metaplasticity is essential for navigation of experience-rich natural environments.     

The ecological significance of time sense in animals

Time is a fundamental dimension of all biological events and it is often assumed that animals have the capacity to track the duration of experienced events (known as interval timing). Animals can potentially use temporal information as a cue during foraging, communication, predator avoidance, or navigation. Interval timing has been traditionally investigated in controlled laboratory conditions but its ecological relevance in natural environments remains unclear. While animals may time events in artificial and highly controlled conditions, they may not necessarily use temporal information in natural environments where they have access to other cues that may have more relevance than temporal information. Herein we critically evaluate the ecological contexts where interval timing has been suggested to provide adaptive value for animals. We further discuss attributes of interval timing that are rarely considered in controlled laboratory studies. Finally, we encourage consideration of ecological relevance when designing future interval-timing studies and propose future directions for such experiments.