Bird predation, sexual segregation and fission-fusion societies: the amazing noctules (vesper bats part XIX)

I find myself astonished by the fact that I've done it. With the publication of this article I've succeeded in providing a semi/non-technical overview of all the vesper bats of the world... or, of all the major lineages, anyway. Obviously, it hasn't been possible to even mention all 400-odd vesper bat species, let alone all the 'species groups' suggested for the more speciose genera, but I think I've succeeded in discussing all extant genera, and at least some of the fossil ones too.

As you'll know if you've been following the series, we've moved along the cladogram and now find ourselves within one of the youngest vesper bat clades: the one that contains pipistrelles and noctules. Having looked at the (probably paraphyletic) pipistrelles, it's now time to bring the series to a close by looking at noctules [Common noctule Nyctalus noctula shown here; by Mnolf, from wikipedia]. After this there's an article on conservation and vesper bat decline. It's pretty grim reading, but it's also very important.

Noctules (Nyctalus) are my favourite vesper bats. These large, Old World, woodland bats have relatively long, narrow wings and high wing loadings; their dark faces are short (they've been described on occasion as 'pug-nosed') and their fur is sleek and gives them a streamlined look. Some species have a golden brown or yellowish brown pelt. The biggest of them - the Greater noctule N. lasiopterus - reaches 75 g and can have a wingspan of 45 cm, making it the largest bat in Europe and one of the largest of all vesper bats: I said in the serotine article that the Great evening bat Ia io is the largest vesper bat of all but had forgotten at the time that the Greater noctule can apparently exceed it in mass (though not in wingspan). The biggest Great evening bats weigh 63 g and have wingspans of about 51 cm. [Adjacent photo shows N. azoreum; by Filipe Lopes, from wikipedia].

The 6-8 currently recognised noctule species range across most of Europe, northern Africa and Asia, and also occur on the Azores and the Canary Islands. Three species have partially overlapping ranges in Europe: the Common noctule, Greater noctule and Leisler's bat or Lesser noctule N. leisleri. Afghanistan, India and Nepal are inhabited by the poorly known Mountain noctule N. montanus while north-east Asia is home to the Birdlike noctule N. aviator [shown below; from here]. So far as I can tell, it isn't any more bird-like than other noctule. Two additional east Asian species (Japanese noctule N. furvus and Chinese noctule N. plancyi) are recognised by some authors.

The best known of them - often just termed the Noctule but also referred to as the Common noctule - has recently (post-1997) been recorded as a first-time breeding species in Spain, France, Baden-Württemberg and Bavaria, Austria, Italy and Slovakia. It might be expanding its range, though increased research and improved communication might also explain this apparent increase.

The endemic Azorean species - N. azoreum [shown up the page, above the N. aviator photo] - is of special interest in exhibiting more diurnal activity than is typical for a bat (Moore 1975). This is presumably due to 'release' from avian predation though, interestingly, the species still exhibits clustering behaviour when emerging from its roosts ('clustering' describes the behaviour when bats emerge rapidly in clumps of several individuals: individuals never emerge on their own) (Irwin & Speakman 2003). Clustering in other bats may not, therefore, necessarily be an anti-predator adaptation (though the alternative possibilities that Azorean noctules exhibit clustering as a sort of tradition or because they still need to be wary of predation from such animals as rats and cats have also been considered).

Formidable predators of mice and birds

Due in part to their comparatively large size, noctules often prey on large insects like beetles and moths, and there are even accounts of the Common noctule preying on mice. One of the most remarkable discoveries made about any bat (in my opinion) is that the Greater noctule catches and eats migrating passerines, including Robin Erithacus rubecula and Wood warbler Phylloscopus sibilatrix (Dondini & Vergari 2000). This has been the cause of debate in the literature, with some authors arguing that claims of bird-eating in this species must be mistaken. Surely, they argue, the supposed evidence can be explainable via some other means (such as the accidental ingestion of falling feathers (Bontadina & Arlettaz 2003)) [adjacent figure - from Dondini & Vergari (2000) - shows how significant feathers and bird bones are as a percentage of Greater noctule droppings (at least, during September, October and November)].

The presence of bird bone fragments in Greater noctule droppings, of cut passerine wings beneath freshly-netted Greater noctules, and of Robin feathers found adhering to the claws of netted Greater noctules, demonstrates pretty convincingly that these bats really are catching nocturnally migrating birds, and their flight and echolocation style, overall size and wing loadings all indicate that this predatory behaviour is certainly plausible (Ibáñez et al. 2001). Once again, this behaviour has yet to be photographed or filmed, nor has anyone thought to illustrate it (so far as I can tell). In desperation I therefore produced another vesper bat vs passerine sketch - I'm not entirely happy with it, would look better if it were coloured.

It's assumed that the noctules catch small birds in the same way as they do insects: by encircling the prey with both the wings and the large tail membrane before biting it to death and consuming it on the wing, at altitude (Popa-Lisseanu et al. 2007). We have to consider the idea that vesper bats that overlap with noctules in planform, size and foraging behaviour could well be bird-killers too: I noted this when writing about the bird-killing behaviour of the Greater noctule in 2006 (there's a chapter on it in Tetrapod Zoology Book One... oh look, shown here), and since then bird-eating has been discovered in the Great evening bat (see the serotine article for more).

Noctules look, essentially, like giant pipistrelles and, as we saw in the previous article on pipistrelles, this may be exactly what they are. If so, pipistrelles in the strict sense span a phenomenal amount of variation, with small species (like Pipistrellus pygmaeus) sometimes being adult at just 4 g while the biggest ones (like the Greater noctule) reach weights of 75 g (Hulva et al. 2010). Two species currently included in Hypsugo (and hence regarded as hypsugines) - H. joffrei from Myanmar and H. stenopterus from south-east Asia - have been included in Nyctalus by some authors: if correct, this would increase the Asian range of the group to the south-east. I don't think it is correct, however.

Sexual segregation, singing and highly structured fission-fusion societies

In some respects, noctule social behaviour is quite similar to that of pipistrelles (see the previous article), probably not coincidentally. Noctules are mostly tree-hole roosters (some roosts are as little as 1 m above ground level) but they do use buildings in some areas (particularly continental Europe).

As in pipistrelles, it seems common for males to mostly live alone during the summer (though they do sometimes form small bachelour groups) and for males and females to meet up as males form breeding territories in late summer and autumn. Males sing from within these territories, typically from a perch close to the roost entrance, though Leisler's bat at least has been known to sing in flight. Use of the same 'song perch' night after night has been recorded for Leisler's bat. Not only do males emit shrill calls that attract females, they also produce a strong odour. Successful males end up with a harem of up to 18 females. The females stay with the male for just one or two days before moving on.

Segregation of the sexes is common in noctules, as it is in temperate vesper bats in general, but it seems that different patterns occur in different regions. In northern Spain, Ibáñez et al. (2009) showed that female Common noctule and Leisler's bat dispersed well away from males via long-distance migration, resulting in substantial geographical segregation of the sexes. This is interesting because massive segregation of the sexes (as in, being separated by the width of a whole country) is well known in the highly migratory Hoary bat Lasiurus cinereus in North America (one of the hairy-tailed bats): the degree of segregation seen in that bat is mightily impressive, but maybe it isn't so unique after all. However, Ibáñez et al. (2009) showed that noctules were pretty flexible in terms of movement and segregation. Female Greater noctules in northern Spain also moved away from males, but the segregation was via altitude, not distance, while female Common noctule and Leisler's bat in southern Spain only moved a short distance from males, essentially staying within the same area. [Adjacent Greater noctule photo from Popa-Lisseanu et al. (2007)].

Within the maternity roosts, females leave their babies in crèches while they go out to forage. They often roost-switch, carrying the baby with them of course. Various different ideas have been put forward to explain roost-switching: perhaps the bats move to avoid parasites, perhaps they want to move to more productive foraging areas, or perhaps they need to keep tabs on the resources around the general roost area. In the Greater noctule, Popa-Lisseanu et al. (2007) showed how the movements of individuals are best explained by the maintenance of social bonds with other colony members: it seems that long-term social structures persist for decades in maternity roosts, with related females being loyal to roosts and with young females tending to return to the social group they were born into. This is a flexible, so-called fission-fusion society of the sort seen elsewhere in lions, chimps, spotted hyenas and bottlenose dolphins.

Winter colonies can consist of hundreds of tightly huddled individuals, typically packed into hollow trees. In cooler regions, some of the species migrate for anything up to 2000 km, but other populations stay put and hibernate through cold winters.

And, with that, we are done with noctules, and done with vespertilionins, and done with the vesper bats. One more article in the series to come though. And here are some cladograms again, to remind you where we are and what we've seen...

For previous Tet Zoo articles in the vesper bats series, see...

• Introducing the second largest mammalian 'family': vesper bats, or vespertilionids
• The vesper bat family tree: of myotines, plecotins, antrozoins, and all those cryptic species (vesper bats part II)
• Bent-winged bats: wide ranges, very weird wings (vesper bats part III)
• Of southern African wing-gland bats, woolly bats, and the ones with tubular nostrils (vesper bats part IV)
• The many, many mouse-eared bats, aka little brown bats, aka Myotis bats (vesper bats part V)
• Long-eared bats proper: Plecotus and other plecotins (vesper bats part VI)
• Desert long-eared bats - snarling winged gremlins that take scorpion stings to the face and just don't care (vesper bats part VII)
• Hairy-tailed bats: a tale of furry tails, red coats, cold tolerance, migration and sleeping out in the open (vesper bats part VIII)
• Robust jaws and a (sometimes) 'greenish' pelt: house bats (vesper bats part IX)
• Australasian big-eared bats, and how to (perhaps) single-handedly wipe out an entire species, 1890s-style (vesper bats part X)
• Antrozoins: pallid bats, Van Gelder's bat, Rhogeessa... Baeodon!! (vesper bats part XI)
• Putting the 'perimyotines' well away from pips proper (vesper bats part XII)
• Nycticein bats: apparently, a nice example of how assorted distant relatives can be mistakenly considered close allies on the basis of one or two characters (vesper bats part XIII)
• Eptesicini: the serotines and their relatives (vesper bats part XIV)
• Hypsugines: an assemblage of 'pipistrelle-like non-pipistrelles' (vesper bats part XV)
• A list of enigmas: bamboo bats, frogs-head flyers, Rohu's bat and the false serotines (vesper bats part XVI)
• Lobed bats, butterfly bats, particoloured bats, thick-thumbed bats, Dormer's bats, bats, bats, BATS... did I mention the bats? (vesper bats part XVII)
• Pipistrelles proper: little bats that glide, sing, swarm and lek (vesper bats part XVIII)

And for previous Tet Zoo articles on bats, see...

• Desmodontines: the amazing vampire bats
• Giant extinct vampire bats: bane of the Pleistocene megafauna
• Camazotz and the age of vampires
• Dark origins: the mysterious evolution of blood-feeding in bats
• A new hypothesis on the evolution of blood-feeding: food source duality involving nectarivory. Catchy, no?
• Oh no, not another giant predatory flightless bat from the future
• The most terrestrial of bats
• I stroked a pipistrelle
• Red bats
• We flightless primates
• Big animalivorous microbats
• Hidden in plain sight: discovering cryptic vesper bats in the European biota
• PROTOBATS: visualising the earliest stages of bat evolution

Refs - -

Bontadina, F. & Arlettaz, R. 2003. A heap of feathers does not make a bat's diet. Functional Ecology 17, 141-145.

Dondini, G., & Vergari, S (2000). Carnivory in the greater noctule bat (Nyctalus lasiopterus) in Italy. Journal of Zoology, 251, 233-236

Hulva, P., Fornůskova, A., Chudárková, A., Evin, A., Allegrini, B., Benda, P. & Bryja, J. 2010. Mechanisms of radiation in a bat group from the genus Pipistrellus inferred by phylogeography, demography and population genetics. Molecular Ecology 19, 5417-5431.

Ibáñez, C, Guillén, A., Agirre-Mendi, P. T., Juste, J., Schreur, G., Cordero, A. I. & Popa-Lisseanu, A. G. 2009. Sexual segregation in Iberian noctule bats. Journal of Mammalogy 90, 235-243.

- ., Juste, J., GarcÃa-Mudarra, J. L. & Agirre-Mendi, P. T. 2001. Bat predation on nocturnally migrating birds. Proceedings of the National Academy of Sciences 98, 9700-9702.

Irwin, N. R. & Speakman, J. R. 2003. Azorean bats Nyctalus azoreum, cluster as they emerge from roosts, despite the lack of avian predators. Acta Chiropterologica 5, 185-192.

Moore, N. W. 1975. The diurnal flight of the Azorean bat (Nyctalus azoreum) and the avifauna of the Azores. Journal of Zoology 177, 483-506.

Popa-Lisseanu, A. G., Bontadina, F., Mora, O. & Ibañez, C. 2008. Highly structured
ï¬ssion-fusion societies in an aerial-hawking, carnivorous bat. Animal Behaviour 75, 471-482.

- ., Delgado-Huertas, A., Forero, M. G., Rodriguez, A., Arlettaz, R. & Ibáñez, C. 2007. Bats' conquest of a formidable foraging niche: the myriads of nocturnally migrating songbirds. PLoS ONE 2(2): e205. doi:10.1371/journal.pone.0000205