Friday, July 3, 2009

On the Importance of Vultures


Torgos - of no relation to Manos. Taken from here.


Our anthropocentric stigma against scavengers is totally underserved and in fact, carrion consumption is a valuable ecological "service". The word "scavenger" is used fast and loose in popular parlance but the label should be restricted to animals which depend heavily on carrion; just about every vertebrate which can consume meat (including many "herbivores") won't hesitate to snack on a corpse here and there - even humans. The three independent lineages of vultures have specialized for locating and feeding on carrion and utilize the resource to the degree that they can be known as "obligate scavengers" - although it should be noted that it is not their sole food source.

Just to get the word out, nothing said in this article applies to the so-called "Palm-nut vulture" Gypohierax angolensis which is specialized for eating palm nuts (!) and feeds on fish (!!), live prey, and then carrion to a lesser extent (Mundy et al. 1992). Gypohierax is closely related to the gypaetine vultures (both fairly aberrant)... but also Polyboroides and Eutriorchis (Griffiths et al. 2007, Lerner and Mindell 2005). Oh, and the whole "New World"/"Old World" schism is a false dichotomy as these vultures didn't pay attention to those biogeographical rules earlier in their evolution. Anyways, back to the post:


Carrion is an ephemeral and unpredictable resource so it is no surprise that the vertebrates which depend on it the most can fly. Vultures all have large wingspans and locomote by soaring flight (Ruxton and Houston 2004); their stomach acid has a very low pH (1) and is apparently capable of resisting/detoxifying bacteria (Sekercioglu 2006); bald heads and necks don't correlate well with messy feeding habits (contra Mundy et al. 1992) but function along with postural changes as a thermoregulatory mechanism vital to these birds which may deal with rapidly-changing temperatures ranging from <0>70 °C (due to altitude) (Ward et al. 2008). Hertel (1995) outlined the morphological traits shared by these lineages: the long, narrow, shallow, and highly curved maxilla is designed for hooking or slicing large chunks of meat (comparable in function to a meathook); the deep ramus is an adaptation for dorsoventral forces correlated with rapid consumption; there is a large angle between the foramen magnum and basicranium reflecting the strait line of pulling force of the head and neck (avivores, in comparison, have an angle approaching 90 degrees); the narrow ramus and shallow mandibular symphysis indicate a lack of resistance to struggling prey; the occipital distance is greater and orbits are smaller (scavengers are less dependant on eyesight, apparently).


First: Accipiter cooperi - modified from here. This species is a functional avivore and contrasts strongly in form and function with the scavenger lineages. Hertel (1995) compared them to staplers or churchkey can openers function-wise.
Second: Neophron percnopterus - modified from here. A member of the gypaetine vulture lineage(s?). Skull indices of this species and one of its extinct North American relatives (Neophrontops americanus) are well into the "scavenger" ecomorph range despite the extant species taking a broad range of food in addition to carrion (Hertel 1995, Mundy et al. 1992).
Third: Gyps tenuirostris - modified from here. An aegypiine vulture - of all the 13 species in this lineage the 8 Gyps are the most specialized for scavenging (Mundy et al. 1992).
Fourth: Coragyps atratus - modified from here. A member of the cathartid lineage; they're distant relatives of the other vulture lineages but it isn't clear to what degree.


Although functionally similar, there are distinct lineages of gypaetine, aegypiine, and cathartid vultures. The birds which can be called gypaetine vultures are abarrent scavengers; Gypaetus barbatus feeds mostly on bone marrow (it appears to retain vulture-like skull indices despite this); Neophron percnopterus keeps a low profile at large mammal carcasses, is an important small animal scavenger/predator, feeds on eggs, and also consumes fecal matter (preferring carnivore and... human) (Mundy et al 1992). The gypaetine vultures are more basal in the order Falconiformes/Accipitriformes and appear to be allied to the pernine kites; the more familiar aegypiine vultures are more derived and have been recovered in a position somewhere near some of the serpent eagles (long story - see Griffiths et al. 2007 and Lerner and Mindell 2005). Cathartids are, well, certainly not storks and are either basal member of Falconiformes/Accipitriformes (also a long story) or a distinct (ordinal-level?) clade located nearby in a huge mess (see Livezey and Zusi (2007) & Hackett et al. (2008) for the former placement - Morgan-Richards et al. (2008) (and similar mtDNA studies it cites) for the latter).


I think we have been sufficiently introduced to vultures.


So just why is scavenging important? It isn't just some biological curiosity - most animals die from causes unrelated to predation and most of their biomass is consumed by vertebrates (and not microbes and invertebrates) (Devault et al. 2003). Turkey vultures (Cathartes aura) were observed to scavenge every experimentally placed carcass (which wasn't badly decomposed) in a forested environment within three days and vultures on the Serengeti have been observed to consume most of the large, conspicuous carcasses (Devault et al. 2003 - citing Houston 1979, 1986, 1988). So forget the image of vultures cleaning up after lions on the savannah - they consume staggering amounts of biomass from carcasses the size of mice to elephants in temperate and tropical environments worldwide (except Australia...).

It is unfortunate that the loss of Gyps vultures in South Asia due to diclofenac poisoning has demonstrated just how important they were in the ecosystem. The near-extinction of the vultures caused an explosion in the feral dog and rat population and the potential for disease could impact domestic animals and humans (Pain et al. 2003, Prakash et al. 2005). Interestingly, while the importance of facultative scavengers cannot be overstated, these scavengers (such as crows, gulls, starlings) lack the ability to deal with pathogens present in vultures and are more prone to spreading them (Blanco et al. 2006).


Although it appears that vultures are important ecosystem players, facultative scavengers seem to get the job done without them in boreal areas, Australia, and some islands. Perhaps areas with relatively low terrestrial production simply can't support the needs of obligate scavengers and the more generalized species wholly exclude them. The fossil record before the K/T event does not appear to show a community of vulture analogues as none of the pterosaurs and basal birds (that I'm aware of!) show the characteristic skull indices outlined by Hertel (1995) - so presumably a wide variety of facultative scavengers can cover for vultures even in areas with high production. Whatever was going on, in a good portion of our world today vultures are vital parts of the ecosystem and their worldwide decline could be disastrous for a number of as-yet unseen reasons.


Obligate scavengers will even eat facultative scavengers.
Photo taken from here.


References:

Blanco et al. 2006. Faecal bacteria associated with different diets of wintering red kites: influence of livestock carcass dumps in microflora alteration and pathogen acquisition. J. Appl. Ecol. 43, 990–999.

DeVault, Travis L. et al. 2003. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102, 225-234

Hertel, Fritz. 1995. Ecomorphological Indicators of Feeding Behavior in Recent and Fossil Raptors. The Auk 112, 890-903.

Griffiths, Carole S. et al. 2007. Phylogeny, diversity, and classification of the Accipitridae based on DNA sequences of the RAG-1 exon. J. Avon. Biol. 38, 587-602

Hackett, Shannon J. et al. 2008. A Phylogenomic study of Birds Reveals Their Evolutionary History. Science 320, 1763-1768.

Lerner, H. R. L. and Mindell, D. P. 2005. Phylogeny of eagles, Old World vultures, and other Accipitridae based on nuclear and mitochondrial DNA. Mol. Phyl. Evol. 37, 327-346

Livezy, Bradley C. and Zusi, Richard L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool. J. Linn. Soc. 149, 1-95

Morgan-Richards, Mary et al. 2008. Bird evolution: testing the Metaves clade with six new mitochondrial genomes. BMC Evolutionary Biology 8

Mundy, Peter et al. 1992. The Vulture of Africa. Academic Press

Pain, D. et al. 2003. Causes and effects of temporospatial declines of Gyps vultures. Asia. Cons. Biol. 17, 661–671.

Prakash, V. et al. 2005. Catastrophic collapse of Indian white-backed Gyps bengalensis and long-billed Gyps indicus vulture populations. Biol. Cons. 109, 381–390.

Ruxton, Graeme D. and Houston, David C. 2004. Obligate vertebrate scavengers must be large soaring fliers. Journal of Theoretical Biology 228, 431-436

Sekercioglu, Cagan H. 2006. Increasing awareness of avian ecological functions. TRENDS in Ecology and Evolution 21, 464-471

Ward, Jennifer et al. 2008. Why do vultures have bald heads? The role of postural adjustment and bare skin areas in thermoregulation. Journal of Thermal Biology 33, 168-173.

Whelan, Christopher J. et al. 2008. Ecosystem services provided by birds. Annals of the New York Academy of Sciences 1134, 25-60

7 comments:

Allen Hazen said...

Definite change of pace from after the cryptofish, but nice post: I think a lot of people would learn something worth knowing from it!

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Interesting, I didn't know there were no vultures in Australia.

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