Proximity sensors reveal social information transfer in maternity colonies of Common noctule bats

Bats are a highly gregarious taxon suggesting that social information should be readily available for making decision. Social information transfer in maternity colonies might be a particularly efficient mechanism for naïve pups to acquire information on resources from informed adults. However, such behaviour is difficult to study in the wild, in particular in elusive and small-bodied animals such as bats. The goal of this study was to investigate the role of social information in acquiring access to two types of resources, which are crucial in the life of a juvenile bat: suitable roosting sites and fruitful feeding grounds. We hypothesized that fledging offspring will make use of social information by following informed members of the social groups to unknown roosts or foraging sites. In the present study we applied for the first time the newly developed miniaturized proximity sensor system ‘BATS’, a fully automated system for documenting associations among individual bats both while roosting and while on the wing. We quantified associations among juveniles and other group member while switching roosts and during foraging. We found clear evidence for information transfer while switching roosts, mainly among juveniles and their genetically identified mothers. Anecdotal observations suggest intentional guidance behaviour by mothers, indicated by repeated commuting flights among the pup and the target roost. Infrequent, short meetings with colony members other than the mother indicate local enhancement at foraging sites, but no intentional information transfer. Our study illustrates how advances in technology enable researchers to solve long-standing puzzles. Miniaturized proximity sensors facilitate the automated collection of continuous data sets and represent an ideal tool to gain novel insights into the sociobiology of elusive and small-bodied species.

[1]  M. Knörnschild,et al.  Postweaning maternal food provisioning in a bat with a complex hunting strategy , 2013, Animal Behaviour.

[2]  E. Kalko,et al.  Calls in the Forest: A Comparative Approach to How Bats Find Tree Cavities , 2009 .

[3]  Caroline Schuppli,et al.  The Ecology of Social Learning in Animals and its Link with Intelligence , 2016, The Spanish Journal of Psychology.

[4]  G. Wilkinson,et al.  Social calls coordinate foraging in greater spear-nosed bats , 1998, Animal Behaviour.

[5]  O. V. Helversen,et al.  EXTRA-HAREM PATERNITY IN THE WHITE-LINED BAT SACCOPTERYX BILINEATA (EMBALLONURIDAE) , 1999 .

[6]  P. Ward,et al.  THE IMPORTANCE OF CERTAIN ASSEMBLAGES OF BIRDS AS “INFORMATION‐CENTRES” FOR FOOD‐FINDING , 2008 .

[7]  Erick Greene,et al.  Allometry of Alarm Calls: Black-Capped Chickadees Encode Information About Predator Size , 2005, Science.

[8]  Gerald Kerth,et al.  Information transfer about roosts in female Bechstein's bats: an experimental field study , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[9]  G. Kerth,et al.  Similar is not the same: Social calls of conspecifics are more effective in attracting wild bats to day roosts than those of other bat species , 2010, Behavioral Ecology and Sociobiology.

[10]  H. Schnitzler,et al.  From spatial orientation to food acquisition in echolocating bats , 2003 .

[11]  D. Kleiman Maternal care, growth rate, and development in the noctule (Nyctalus noctula), pipistrelle (Pipistrellus pipistrellus), and serotine (Eptesicus serotinus) bats , 1969 .

[12]  Robert Weigel,et al.  Automated proximity sensing in small vertebrates: design of miniaturized sensor nodes and first field tests in bats , 2016, Ecology and evolution.

[13]  Robert Weigel,et al.  Enhanced mobile node design for small size animal borne wireless sensor nodes with encounter detection and localization , 2018, 2018 11th German Microwave Conference (GeMiC).

[14]  J. Altringham,et al.  Development of conserved microsatellite markers of high cross‐species utility in bat species (Vespertilionidae, Chiroptera, Mammalia) , 2012, Molecular ecology resources.

[15]  Anne-Béatrice Dufour,et al.  The ade4 Package: Implementing the Duality Diagram for Ecologists , 2007 .

[16]  D. Grünbaum,et al.  BLACK-BROWED ALBATROSSES FORAGING ON ANTARCTIC KRILL: DENSITY-DEPENDENCE THROUGH LOCAL ENHANCEMENT? , 2003 .

[17]  Gerald S. Wilkinson,et al.  Social grooming in the common vampire bat, Desmodus rotundus , 1986, Animal Behaviour.

[18]  Sasha R. X. Dall,et al.  Information use in colonial living , 2016, Biological reviews of the Cambridge Philosophical Society.

[19]  J. Lindström,et al.  Early development and fitness in birds and mammals. , 1999, Trends in ecology & evolution.

[20]  Gerald S. Wilkinson,et al.  Food Sharing in Vampire Bats , 1990 .

[21]  Iris I. Levin,et al.  Performance of Encounternet Tags: Field Tests of Miniaturized Proximity Loggers for Use on Small Birds , 2015, PloS one.

[22]  H. Broders,et al.  Who swarms with whom? Group dynamics of Myotis bats during autumn swarming , 2015 .

[23]  Lars Chittka,et al.  Social Learning in Insects — From Miniature Brains to Consensus Building , 2007, Current Biology.

[24]  Shirley A. Miller,et al.  A simple salting out procedure for extracting DNA from human nucleated cells. , 1988, Nucleic acids research.

[25]  Gerald S. Wilkinson,et al.  Information transfer at evening bat colonies , 1992, Animal Behaviour.

[26]  M. Knörnschild,et al.  Complex vocal imitation during ontogeny in a bat , 2010, Biology Letters.

[27]  Gerald Kerth,et al.  Causes and Consequences of Sociality in Bats , 2008 .

[28]  B. Siemers,et al.  The sensory basis of roost finding in a forest bat, Nyctalus noctula , 2007, Journal of Experimental Biology.

[29]  Richard James,et al.  Calibrating animal‐borne proximity loggers , 2015, Methods in ecology and evolution.

[30]  S. Kalinowski,et al.  Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment , 2007, Molecular ecology.

[31]  Kamran Safi,et al.  Experimental evidence for group hunting via eavesdropping in echolocating bats , 2009, Proceedings of the Royal Society B: Biological Sciences.

[32]  G. Jones Ontogeny, functional ecology, and evolution of bats: The ontogeny of behavior in bats: a functional perspective , 2000 .

[33]  G. Jones Ontogeny, Functional Ecology, and Evolution of Bats , 2002 .

[34]  Arjan Boonman,et al.  Bats Aggregate to Improve Prey Search but Might Be Impaired when Their Density Becomes Too High , 2015, Current Biology.

[35]  Gavin Simpson,et al.  Analogue Methods in Palaeoecology: Using the analogue Package , 2007 .

[36]  John M Ratcliffe,et al.  Roosts as information centres: social learning of food preferences in bats , 2005, Biology Letters.

[37]  V. Castella,et al.  Characterization of highly variable microsatellite loci in the bat Myotis myotis (Chiroptera: Vespertilionidae) , 2000, Molecular ecology.

[38]  T. Clutton‐Brock,et al.  The Evolution of Parental Care , 2019 .

[39]  Martin Wikelski,et al.  50 years of bat tracking: device attachment and future directions , 2014 .

[40]  Sigal Balshine,et al.  Patterns of parental care in vertebrates , 2012 .

[41]  T. Clutton‐Brock,et al.  Early development, survival and reproduction in humans , 2002 .

[42]  P. Prodöhl,et al.  Development and characterization of 11 polymorphic compound tetranucleotide microsatellite loci for the Leisler’s bat, Nyctalus leisleri (Vespertilionidae, Chiroptera) , 2009, Conservation Genetics.

[43]  M. Knörnschild,et al.  Social influences on territorial signaling in male greater sac-winged bats , 2013, Behavioral Ecology and Sociobiology.

[44]  K. Gibson,et al.  Mammalian social learning : comparative and ecological perspectives , 1999 .

[45]  E. Gillam,et al.  Social calls used by a leaf-roosting bat to signal location , 2010, Biology Letters.

[46]  C. Moss,et al.  Pup guarding by greater spear-nosed bats , 2009, Behavioral Ecology and Sociobiology.

[47]  Thomas H. Kunz,et al.  Ecological and behavioral methods for the study of bats, 2nd edition , 2009 .

[48]  L. Giraldeau,et al.  Social influences on foraging in vertebrates: causal mechanisms and adaptive functions , 2001, Animal Behaviour.

[49]  E. Gillam Eavesdropping by bats on the feeding buzzes of conspecifics , 2007 .

[50]  T. Kunz,et al.  A call-and-response system facilitates group cohesion among disc-winged bats , 2013 .

[51]  Richard James,et al.  Experimental resource pulses influence social-network dynamics and the potential for information flow in tool-using crows , 2015, Nature Communications.

[52]  Rüdiger Kapitza,et al.  Automated Encounter Detection for Animal-Borne Sensor Nodes , 2017, EWSN.

[53]  R. Kays,et al.  Terrestrial animal tracking as an eye on life and planet , 2015, Science.

[54]  Sasha R. X. Dall,et al.  Information and its use by animals in evolutionary ecology. , 2005, Trends in ecology & evolution.

[55]  G. Kerth,et al.  How Do Young Bats Find Suitable Swarming and Hibernation Sites? Assessing the Plausibility of the Maternal Guidance Hypothesis Using Genetic Maternity Assignment for two European Bat Species , 2017, Acta Chiropterologica.

[56]  D. Rubenstein,et al.  Comparative Social Evolution , 2017 .

[57]  E. I. Kozhurina Social Organization of a Maternity Group in the Noctule Bat, Nyctalus noctula (Chiroptera: Vespertilionidae) , 2010 .

[58]  Dina K. N. Dechmann,et al.  Frugivorous bats evaluate the quality of social information when choosing novel foods , 2014 .