1. Ecology

Behavior: Flying squirrels, hidden treasures

In the rain forests of Hainan, China, two species of squirrel create grooves on the surface of smooth nuts so that they can wedge them in the forks between branches.
https://doi.org/10.7554/eLife.89823
Share this article
Cite this article
  1. Pizza Ka Yee Chow
(2023)
Behavior: Flying squirrels, hidden treasures
eLife 12:e89823.
https://doi.org/10.7554/eLife.89823
  2. Download BibTeX
  3. Download .RIS
  1. Pizza Ka Yee Chow  Is a corresponding author
  1. School of Psychology at the University of Chester, United Kingdom

Just how we may stash away precious chocolate bars for future cravings, many animals hoard food to prepare for times of low supply (Vander Wall, 1990). Tree squirrels, for instance, are well known for employing this strategy. Some, like the American red and Douglas squirrels, are predominantly ‘larder hoarders’ who tend to store nuts and seeds in one dedicated spot, called a midden (Steele, 1998; Steele, 1999). Others, like the Eurasian red squirrels and Eastern grey squirrels, tend to be ‘scatter hoarders’ who cache their items one by one in tree cavities, between logs, or inside holes in the ground (Smith, 1968; Wauters and Casale, 1996). Now, in eLife, Suqin Fang and colleagues from institutes in China and Canada — including Han Xu and Lian Xia as joint first authors — report a surprising hoarding strategy employed by certain Chinese populations of flying squirrels (Xu et al., 2023).

Xu et al. accidentally discovered this caching behaviour when conducting fieldwork in Hainan Island, China. Amongst the shrubs and saplings of the Hainan Tropical Rainforest National Park, they began to notice that many nuts from Cyclobalanopsis trees were ‘stuck’ within the fork present between diverging twigs. The smooth, oval-shaped nuts showed a spiral groove around their middle section, as well as chew marks of more varied depths towards their bottom end.

Intrigued, the team conducted three systematic field searches and set trail cameras to record animal activity around the clock. After months of work, a few images and videos revealed that two species of flying squirrels, Hylopetes phayreielectilis and Hylopetes alboniger (commonly known as the Indochinese and the particolored flying squirrels), were responsible for making these grooves and affixing the nuts (Figure 1).

Figure 1
Download asset Open asset
Food hoarding behaviour of two flying squirrel species, Hylopetes phayreielectilis and Hylopetes alboniger in Hainan Island, China.

Upon finding a nut from the Cyclobalanopsis tree, two out of the nine species of flying squirrels present in Hainan rainforests make a spiral groove around the middle of the nut (top), as well as grooves at its bottom (bottom), before fixing it in the fork of twigs. This hoarding strategy may help to preserve the nuts for longer in this demanding, humid environment.

Importantly, this work suggests that the behaviour could represent an adaptive response to the demands of tropical forests. Tree squirrels face many challenges when it comes to hoarding their food, such as competitors that pilfer their stocks or environmental conditions that may degrade stored items. In response, they have developed a range of pre- and post-hoarding behaviours to minimise food loss (Robin and Jacobs, 2022). For example, to stop seeds and nuts from sprouting, American red squirrels store cones away from the soil in their middens while Eastern grey squirrels remove the structures responsible for germination from their acorns prior to hiding them (Steele et al., 2001; Vander Wall, 1990). Xu et al. noted that Cyclobalanopsis nuts would remain intact for several months once lodged within forks, whereas they germinate in two to three months when on the ground of tropical rainforests (Zhou, 2001).

Arguably, suspended nuts are there for all to see; this can result in thieving, a major social challenge that can lead hoarders to lose 30% of their food per day (Vander Wall, 1990; Vander Wall and Jenkins, 2003). The team recorded several types of behaviour that could help to minimize pilferage, including the animals often storing their nuts away from the tree where they had found them. Caches were also regularly visited by squirrels – a habit that could allow them to relocate items away from compromised locations, for example. Without knowing for certain that the same animal was both storing and checking on a particular nut, however, it is difficult to confirm that this indeed a post-hoarding strategy against thieves. Specifically identifying individuals in future field studies could help to better understand the factors that influence decision-making and behaviour before and after hoarding.

Many species of squirrel play a crucial role for forests, yet flying squirrels have often received less attention (Koprowski and Nandini, 2008). The findings by Xu et al. should renew interest in these rodents, as well as open new avenues of research in behavioural ecology and animal cognition. For example, tree squirrels are usually active during the day and recover their hoarded food using spatial memory alongside olfactory or visual cues; it is unclear if flying squirrels, which are active during the night, use these strategies as well (Gould, 2017; Li et al., 2018). It would also be interesting to investigate whether regularly visiting hoards serves as memory reinforcement to facilitate future recovery, as it is the case for other scatter-hoarding rodents such as agoutis (Hirsch et al., 2013). And finally, an exciting question remains unanswered: does grooving and affixing the nuts rely on trial-and-error and predisposed innate behaviours, or does it require planning and other advanced cognitive processes? More longitudinal observations and systemic experiments in the field will be needed to reveal the intricacies of this behaviour, and how it interacts with the demands of the environment.

References

  1. Book
    1. Gould KL
    (2017) Spatial memory in food-hoarding animals
    In: John HB, editors. Learning and Memory: A Comprehensive Reference. Academic Press. pp. 285–307.
    https://doi.org/10.1016/B978-0-12-809324-5.21016-X
    1. Koprowski JL
    2. Nandini R
    (2008)
    Global hotspots and knowledge gaps for tree and flying squirrels
    Current Sciences 95:851–856.
  10. Book
    1. Vander Wall SB
    (1990)
    Food Hoarding in Animals
    University of Chicago Press.
  14. Book
    1. Zhou T
    (2001)
    Cultivation Techniques of Main Tropical Economic Trees in China
    Chinese Forestry Publishing House.

Article and author information

Author details

  1. Pizza Ka Yee Chow

    Pizza Ka Yee Chow is in the School of Psychology at the University of Chester, Chester, United Kingdom
    For correspondence
    p.chow@chester.ac.uk
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8208-592X

Publication history

  1. Version of Record published: July 7, 2023 (version 1)

Copyright

© 2023, Chow

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 485
    views
  • 31
    downloads
  • 0
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Pizza Ka Yee Chow
(2023)
Behavior: Flying squirrels, hidden treasures
eLife 12:e89823.
https://doi.org/10.7554/eLife.89823

Categories and tags

    1. Related to

    Flying squirrels use a mortise-tenon structure to fix nuts on understory twigs

    Han Xu, Lian Xia ... Suqin Fang
  2. Further reading

Further reading

    1. Ecology

    Flying squirrels use a mortise-tenon structure to fix nuts on understory twigs

    Han Xu, Lian Xia ... Suqin Fang
    Research Article Updated

    Squirrels of temperate zones commonly store nuts or seeds under leaf litter, in hollow logs, or even in holes in the ground; however, in the humid rainforests of Jianfengling in Hainan, South China, we show that some flying squirrels cache elliptical or oblate nuts by hanging them securely in vegetation. These small flying squirrels were identified as Hylopetes phayrei electilis (G. M. Allen, 1925) and Hylopetes alboniger (Hodgson, 1870), in video clips captured of their behavior around focal nuts. Squirrels chewed grooves encircling ellipsoid nuts or distributed on the bottoms of oblate nuts, and then used these grooves to fix nuts tightly between small twigs 0.1–0.6 cm in diameter that were connected at angles of 25–40°. The grooves carved on the nuts (concave structure) connected with Y-shaped twigs (convex structure) and thus firmly affixed the nuts to the plant in a way similar to a mortise-tenon joint used in architecture and carpentry. Cache sites were on small plants located 10–25 m away from the closest potentially nut-producing tree, a behavior that likely reduces the discovery and consumption of the nuts by other animals. The adaptive squirrel behavior that shapes and fits nuts between twigs seems to be directed at providing more secure storage that increases food supply during dry periods in a humid tropical rainforest. In addition to providing such benefits for the squirrels, we suggest that this behavior also impacts the distribution of tree species in the forest.

    1. Ecology

    Adipokinetic hormone signaling mediates the enhanced fecundity of Diaphorina citri infected by ‘Candidatus Liberibacter asiaticus’

    Jiayun Li, Paul Holford ... Xiaoge Nian
    Research Article

    Diaphorina citri serves as the primary vector for ‘Candidatus Liberibacter asiaticus (CLas),’ the bacterium associated with the severe Asian form of huanglongbing. CLas-positive D. citri are more fecund than their CLas-negative counterparts and require extra energy expenditure. Therefore, understanding the molecular mechanisms linking metabolism and reproduction is of particular importance. In this study, we found adipokinetic hormone (DcAKH) and its receptor (DcAKHR) were essential for increasing lipid metabolism and fecundity in response to CLas infection in D. citri. Knockdown of DcAKH and DcAKHR not only resulted in the accumulation of triacylglycerol and a decline of glycogen, but also significantly decreased fecundity and CLas titer in ovaries. Combined in vivo and in vitro experiments showed that miR-34 suppresses DcAKHR expression by binding to its 3’ untranslated region, whilst overexpression of miR-34 resulted in a decline of DcAKHR expression and CLas titer in ovaries and caused defects that mimicked DcAKHR knockdown phenotypes. Additionally, knockdown of DcAKH and DcAKHR significantly reduced juvenile hormone (JH) titer and JH signaling pathway genes in fat bodies and ovaries, including the JH receptor, methoprene-tolerant (DcMet), and the transcription factor, Krüppel homolog 1 (DcKr-h1), that acts downstream of it, as well as the egg development related genes vitellogenin 1-like (DcVg-1-like), vitellogenin A1-like (DcVg-A1-like) and the vitellogenin receptor (DcVgR). As a result, CLas hijacks AKH/AKHR-miR-34-JH signaling to improve D. citri lipid metabolism and fecundity, while simultaneously increasing the replication of CLas, suggesting a mutualistic interaction between CLas and D. citri ovaries.

    1. Ecology

    Human disturbance increases spatiotemporal associations among mountain forest terrestrial mammal species

    Xueyou Li, William V Bleisch ... Xue-Long Jiang
    Research Article

    Spatial and temporal associations between sympatric species underpin biotic interactions, structure ecological assemblages, and sustain ecosystem functioning and stability. However, the resilience of interspecific spatiotemporal associations to human activity remains poorly understood, particularly in mountain forests where anthropogenic impacts are often pervasive. Here, we applied context-dependent Joint Species Distribution Models to a systematic camera-trap survey dataset from a global biodiversity hotspot in eastern Himalayas to understand how prominent human activities in mountain forests influence species associations within terrestrial mammal communities. We obtained 10,388 independent detections of 17 focal species (12 carnivores and five ungulates) from 322 stations over 43,163 camera days of effort. We identified a higher incidence of positive associations in habitats with higher levels of human modification (87%) and human presence (83%) compared to those located in habitats with lower human modification (64%) and human presence (65%) levels. We also detected a significant reduction of pairwise encounter time at increasing levels of human disturbance, corresponding to more frequent encounters between pairs of species. Our findings indicate that human activities can push mammals together into more frequent encounters and associations, which likely influences the coexistence and persistence of wildlife, with potential far-ranging ecological consequences.