The Basking Shark

First off, thanks to Markus Bühler of Bestiarium for inspiring this post by sending me this:

A juvenile basking shark 2.6 m in length from Izawa and Shibata (1993). I was completely unaware of this morphological feature - possible because only a handful of smaller specimens are known. Apparently the elongated snout functions in a similar manner as the cephalic fins of Manta rays.

As the above photo hopefully illustrates, many aspects of basking shark biology remain poorly known. I have a blatant bias towards covering large animals, but given the vulnerability and emerging literature on the animal, I think I can justify this post.

Tracking Basking Sharks

The most interesting aspect of basking shark biology which is now receiving long overdue attention is data on their range and movements. For several decades it was widely assumed (based on very circumstantial evidence) that basking sharks shed their gill rakers and "hibernated" in deep water for the winter! Basking sharks are observed year-round in Monterey Bay, although this population is apparently atypical (Francis and Duffy 2002). Francis and Duffy (2002) analyzed 203 basking shark records (consisting of sightings, captures, and strandings) from New Zealand and determined that basking sharks were swimming in midwater during the winter and did not lose their gillrakers. Sims et al. (2003) used "pop-up" satellite transmitters to gather tracking data for the first time in nearly two decades and directly demonstrated that hibernation does not occur (this study occured off the UK); the study also demonstrated that the sharks traveled extensively vertically and horizontally to productive areas. Skomal et al. (2004) demonstrated that the sharks do not hibernate off the West Atlantic and I think that old hibernation hypothesis can be regarded as completely dead.

Of course, these recent studies have done more than refute the bizarrely widespread hibernation hypothesis. Francis and Duffy (2002) provided unique records of basking sharks 4 km into the brackish Lake Ellesmere - made all the more impressive by (much more common) records of sharks off the continental shelf in water at least 904 m deep. Mancusi et al. (2005) provided the first data on basking sharks from the Eastern Mediterranean and Sandoval-Castillo et al. (2005) provided the first definitive records from Mexico (Pacific coast) - which leads up nicely to Skomal et al. (2009). Skomal et al. (2009) discovered, amazingly, that basking sharks do not have an antitropical distribution as widely assumed previously, but do live in the tropics after all! Sharks tagged off Cape Cod, Massachusetts and found tags in the Sargasso Sea, the Bahamas, Puerto Rican Trench, Caribbean Sea, Guyana, and Brazil - the latter record (a 6480 km trip) is the first transequatorial movement recorded via tagging from a "fish". It seems incredible that a species which was once heavily exploited completely avoided human detection over a considerable portion of its range - it goes to show that basic facts about megafauna are still being discerned. Mitochondrial DNA evidence from Hoelzel et al. (2006) demonstrates that basking sharks have low genetic diversity, a very low worldwide population (effective population ~10,000), and suggested a recent population bottleneck and worldwide panmixia; Skomal et al. (2009) suggested that if basking shark stocks are to recover there will have to be a worldwide effort.

Size & Growth

Since asymptotic size is used for growth calculations, this gives me an excuse to discuss basking shark size. The famous Stronsay carcass was described as a 16.8 m "beast" with all sorts of fanciful features - however its vertebrae were found to correspond exactly in morphology and size with a 9.3 m basking shark (then) recently described by Sir Everard Home (Wood 1982). Wood (1982) mentioned another case where a shark was lashed to the size of a boat and estimated via pacing at ~10.4 m - it was found to be 7.36 m when measured out of the water! Apparently other large figures have been obtained by measuring around the curve of the body. Such is the veracity of basking shark size claims - if a carcass hasn't been scientifically measured in recent decades the data should automatically be categorized as apocryphal.

This by all means doesn't mean that basking sharks aren't huge animals. Francis and Duffy (2002) looked at clasper length in assorted male basking sharks from New Zealand and determined that they reached sexual maturity at ~7.5 m in length; if this is accurate (and it may be somewhat conservative) it means that males in the East Coast region (<>

Anyways, Pauly (2002) used 10 m and ~7.5 tonnes* as an asymptotic size for a von Bertalanffy equation and determined (contra previous studies) that basking sharks do in fact grow very slowly, so slow in fact that they may have a gestation period of 2.6 years. The slow growth also implies considerable longevity (~50 years) and presumably a considerable age at maturity (well over 10 years judging by Figure 4) (Pauly 2002). Estimates of the mortality rate due to the fishery indicates it was impossible for any fish species to withstand for long, particularly one as extremely vulnerable as the basking shark (Pauly 2002). Compagno (2002) notes that in some regions basking sharks numbers have shown no signs of recovery even after decades. It's such a shame that some people are just catching on to this whole "responsibility" thing - hopefully those continuing to hunt the fish in East Asia will figure this out before yet another collapse occurs.

* Wood (1982) cites a 2.99 tonne/7 m individual which scales up to ~8.7 tonnes for 10 m. His 4.65 tonne/7.9 average figure scales up to ~9.4 tonnes for 10 m. I'm guessing that the weight estimation in Pauly (2002) is probably too conservative, but it would be nice to have more data on the subject.

That's about all I want to say about basking sharks. It certainly is remarkable that the biology of a species so heavily exploited could still be a largely emerging picture. Things aren't entirely bleak for the species and fortunately it is getting some good publicity.

References:

Compagno, Leonard J. V. 2002. Sharks of the World. Available (in part)

Francis, M. P. and Duffy, C. 2002. Distribution, seasonal abundance and bycatch of basking sharks (Cetorhinus maximus) in New Zealand, with observations on their winter habitat. Marine Biology 140, 831-842

Hoelzel, A. R. et al. 2006. Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biol. Lett. 2, 639–642. Available

Izawa, Kunihiko and Shibata, Terukazu. 1993. A Young Basking Shark, Cetorhinus maximus, from Japan. Japan J. Ichthyol. 40, 237-245. Available

Mancusi, Cecilia et al. 2005. On the presence of basking shark (Cetorhinus maximus) in the Mediterranean Sea. Cybium 29, 399-405.

Pauly, D. 2002. Growth and mortality of the Basking Shark Cetorhinus maximus and their Implications for Management of Whale Sharks Rhincodon typus. In: Elasmobranch biodiversity: Conservation and Management. Available

Sandoval-Castillo, J. et al. 2005. First record of basking shark (Cetorhinus maximus) in Mexico? JMBA2 - Biodiversity Records

Sims, David W. et al. 2003. Seasonal movements and behaviour of basking sharks from archival tagging: no evidence of winter hibernation. Mar. Ecol. Prog. Ser. 248, 187-196. Available

Skomal, Gregory B. et al. 2004. Archival tagging of a basking shark, Cetorhinus maximus in the western North Atlantic. J. Mar. Biol. Ass. U.K. 84, 1-6.

Skomal, Gregory B. et al. 2009. Transequatorial Migrations by Basking Sharks in the Western Atlantic Ocean. Current Biology 19, 1–4.

Wood, Gerald. 1982. The Guinness Book of Animal Facts and Feats.

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