Fascinated by boobies

Extant sulids - the gannets and boobies - are admittedly pretty uniform (greater diversity existed among fossil forms, as we'll see at some stage), but they still differ in many subtle ways. In the previous sulid post we looked at the gannets: we now turn to the boobies [composite image shown here features Blue-footed booby at top left, Brown booby at bottom left, and Nazca booby at right. All pics from wikipedia].

If you're here because you hadn't realised that 'boobies' was being used in the ornithological sense, sorry. On that subject - everyone knows why the birds are called 'boobies'. What I want to know is - why are the words 'boobs' and 'boobies' used for breasts? Anyway...

The pan-tropical Red-footed booby Sula sula - the most divergent and basal member of Sula according to genetics (Friesen & Anderson 1997, Friesen et al. 2002: cladogram below) - specialises on squids and flying fishes and is markedly nocturnal, with the largest eyes of any sulid. Tropical seas are (usually) low in productivity compared to those closer to the poles, and as a consequence, the Red-footed takes relatively long trips away from its nest. Its reliance on areas of low productivity might also explain why the Red-footed is only able to rear a single chick.

Boobies light and dark

The Red-footed is also a particularly interesting member of the group because it exhibits plumage polymorphism, occurring in an all-white morph, a white-tailed brown morph, and a white-tailed brown morph that also exhibits white scapular feathers (and there are intermediates between these morphs as well) [white and brown morphs shown here, pics from wikipedia]. Plumage polymorphism is rare among seabirds, being exhibited elsewhere only in skuas, in several petrels, and in two storm-petrels. The occurrence of dark morphs in the Red-footed booby is something of a paradox: fish-hunting seabirds are, so it's thought, generally white or white-fronted (or white-bellied) because the white acts as camouflage, disguising the bird against the sky. This was tested by Götmark (1987); the results showed that white-plumaged gulls really did have greater success at catching fish than dark-plumaged ones*. From a fish's point of view an all-dark bird must stand out like a silhouette against a brightly-lit sky. Why, then, be so dark?

* Being white also helps social hunting, as white birds are easier to spot at a distance than dark ones.

Many selection pressures are operating on seabirds besides the need to be camouflaged from prey, and kleptoparasitism from frigatebirds and skuas seems to be an important one (Nelson 1978, Bretagnolle 1993). Nelson (1978) proposed that, in places where kleptoparasitism from frigatebirds was heavy, dark plumage might help boobies to be inconspicuous. Le Corre & Jouventin (1997) and Le Corre (1999) suggested that the dark colour of the Europa boobies (Europa is in the Mozambique Channel) might serve as defensive camouflage given that the dark-morph Red-footed boobies at Europa live alongside large numbers of Great frigatebirds Fregata minor - and are in the wintering range of Southern skua Catharacta antarctica. The Europa boobies are also more gregarious and more nocturnal than Red-footed boobies elsewhere, possibly in response to kleptoparasitism (Le Corre & Jouventin 1997).

However... being dark because it's 'good' for kleptoparasitism avoidance doesn't explain everything, because there are other Red-footed booby populations (like the one on Aldabra, for example) that suffer a great deal from frigatebird kleptoparasitism, yet here the boobies are mostly white. Maybe we need to forget about the hypothesis that some boobies are dark because of kleptoparasitism: maybe thermoregulation, social behaviour or something else is more important (Le Corre 1999). It's also possible that 'colour morphs could have been acquired in a given population by chance or as a result of a 'founding effect', with no selection, if coloration has no impact on the survival of the birds' (Le Corre 1999, p. 414). In connection with this sort of thing, one author said something like 'Perhaps the only generalisation safe to make about animals is that it is unsafe to generalise'. Unfortunately I cannot recall where I read this, nor who said it.

Having mentioned founder [or founding] effects in relation to boobies, it's worth noting that phylogeographic studies indicate how relatively static some sulid populations are. Steeves et al. (2003, 2005a, b) found that both the Isthmus of Panama and the 5400-km-wide Eastern Pacific Basin were significant barriers to gene flow in Masked S. dactylatra, Red-footed and Brown boobies S. leucogaster (all of which have pan-tropical distributions), with populations on either sides of these barriers sharing no, or hardly any, haplotypes*. In the western Indian Ocean, Le Corre (1999) found that the Red-footed booby populations of the various islands were genetically isolated from one another, and that it was this isolation that was helping to maintain the distinction of the various different colour morphs of this species. However, this contrasts with data from the central Pacific, where so much movement seems to occur that there are huge areas where the birds might be considered to form one continuous gene pool (Nelson 1978, Le Corre 1999) [Brown booby shown here, from wikipedia].

* While the genetic data indicates that the Eastern Pacific Basin was a barrier to the dispersal of Brown boobies in the past, members of the species currently seem able to cross the region, with sightings of the eastern subspecies S. l. brewsteri now being reported in the central Pacific, and of the central Pacific (and Indian Ocean) subspecies S. l. plotus now being reported in the eastern Pacific. It is possible that modern geologic or oceanographic changes are preventing the Eastern Pacific Basin from remaining the barrier to dispersal that it once was.

The Masked booby S. dactylatra - a mostly white species with dark brown rectrices and remiges, and of course bluish-black naked facial skin - practises pretty similar foraging behaviour to the Red-foooted booby, but as a larger species than the Red-footed it's able to take larger prey and to dive more deeply. Having discussed some of the mechanics of sulid diving in the previous sulid article, it's worth saying a bit more about what happens once the gannet or booby gets under the water: one might assume that the bird dives with open mouth and aims to catch a particular fish it has been watching during its dive. However, Fisher & Lockley (1989) wrote that a plunge-diving sulid aims to get beneath a fish shoal, and only succeeds in grabbing a prey item on its return to the surface.

Masked and Red-footed boobies both tend to fish offshore. Some boobies are inshore fishers however, in particular the Blue-footed booby S. nebouxii [individual doing courtship display shown here, from wikipedia]. Its small size and particularly long tail allow it to dive within very shallow, inshore waters (sometimes less than 50 cm deep), though it will sometimes dive offshore, particularly the larger females. Blue-footed boobies are particularly interesting in having developed a collaborative fishing technique where members of a group all dive synchronously following a signal - a whistle - given by one individual (usually a male). The Blue-footed booby is closely related to the similar (but grey-footed) Peruvian booby S. variegata, and it appears that the two occasionally hybridise (Figueroa & Stucchi 2008).

The Brown booby also fishes in shallow waters and the small males seem particularly good at this, though less specialised for it morphologically than the Blue-footed (Nelson 1980). Harking back to what we were looking at earlier, the white ventral surface of the Brown booby (explaining its specific name of leucogaster) is presumed to help camouflage it from fish.

Nazca and Tasman boobies

We looked earlier at the Masked booby, a white species that occurs throughout the tropics. It is now generally agreed that a distinctive 'masked booby' population from the Eastern Pacific - known as the Nazca booby - is worthy of specific status, and officially it's now Sula granti (Pitman & Jehl 1998, Friesen et al. 2002). The Nazca booby is smaller and longer-winged than the Masked, with an orange or red (as opposed to yellow) bill and greyer legs; it breeds on the Clipperton and Malpelo islands off Colombia, the Galapagos and La Plata islands off Ecuador, and the Revillagigedo Islands off Mexico, though has also recently been reported from the Lobos de Afuera islands off Peru (Vanderwerf et al. 2008). Nazca boobies are ecologically differentiated from Masked boobies: while the latter preys on flying fish, the former specialises on sardines. It would be interesting to know how the morphological differences reflect these divergent diets. Furthermore, what do these different diets mean for the Masked x Nazca hybrids that have been reported (Vanderwerf et al. 2008)? [Adjacent phylogeny - from Friesen et al. (2002) - shows how haplotypes of Masked (C and B) and Nazca (F) boobies are as distinct as are those of other, conventionally recognised species].

What has been regarded by some authors as a recently extinct species, the Tasman booby S. tasmani, inhabited Lord Howe and Norfolk islands, and apparently became extinct during historical times because of human persecution. Van Tets et al. (1988) first named this species (from bones) in 1988, but they noted how, in its 1788 landing on Lord Howe, the crew of the Supply reported the presence of 'thousands of gannets', all of which were breeding in closely packed nests on the sand. Many birds and eggs were collected for eating (though, unfortunately, no drawings or specimens were retained, so far as we know).

While previously assumed to have been Masked boobies, these birds were breeding in May (Masked boobies breed between September and January), and their habit of nesting in close proximity also makes them different from Masked boobies. As van Tets et al. (1988) stated then, these observations 'may have been the first, last and only record sightings of Sula tasmani' (p. 55). However, other authors (see Priddel et al. 2005, Christidis & Boles 2008) have regarded S. tasmani as conspecific with the Masked booby (some authors have recognised it as a subspecies; others as not worthy of any taxonomic distinction), and it's been argued that the differences in breeding location and so on don't mean much [Masked booby shown in adjacent image, from wikipedia].

The lesson that I get from boobies - and the thing that got me particularly interested in them in the first place - is the obvious fact that subtle morphological and behavioural differences, even in a tightly knit group of very similar species, have led to a lot of interesting diversity, and to so many interesting questions about evolutionary history and the causes of variation. White morphs vs brown morphs, inshore fishers vs offshore fishers, kleptoparasitism avoidance, nocturnality, long tails vs short tails, and sedentary populations vs highly mobile populations. Neat.

Refs - -

Bretagnolle, V. 1993. Adaptive significance of seabird coloration: the case of Procellariiformes. American Naturalist 142, 141-173.

Christidis, L. & Boles, W. 2008. Systematics and Taxonomy of Australian Birds. CSIRO Publishing, Canberra.

Figueroa, J. & Stucchi, M. 2008. Possible hybridization between the Peruvian booby Sula variegataand the Blue-footed booby S. nebouxii in Lodos de Afuera Islands, Peru. Marine Ornithology 36, 75-76.

Fisher, J. & Lockley, R. M. 1989. Seabirds. Bloomsbury Books, London.

Friesen, V. L. & Anderson, D. J. 1997. Phylogeny and evolution of the Sulidae (Aves: Pelecaniformes): a test of alternative modes of speciation. Molecular Phylogentics and Evolution 7, 252-260.

- ., Anderson, D. J., Steeves, T. E., Jones, H. & Schreiber, E. A. 2002. Molecular support for the species status of the Nazca Booby (Sula granti). Auk 119, 820-826.

Götmark, F. 1987. White underparts in gulls function as hunting camouflage. Animal Behaviour 35, 1786-1792.

Le Corre, M. 1999. Plumage polymorphism of red-footed boobies (Sula sula) in the western Indian Ocean: an indicator of biogeographic isolation. Journal of Zoology 249, 411-415.

- . & Jouventin, P. 1997. Kleptoparasitism in tropical seabirds: vulnerability and avoidance responses of a host species, the red-footed booby. Condor 99, 162-168.

Nelson, J. B. 1978. The Sulidae: Gannets and Boobies. Oxford University Press, Oxford.

- . 1980. Seabirds: Their Biology and Ecology. Hamlyn, London.

Pitman, R. L. & Jehl, J. R. 1998. Geographic variation and reassessment of species limits in the "Masked" boobies of the eastern Pacific Ocean. Wilson Society Bulletin 110, 155-170.

Priddel, D., Hutton, I., Olson, S. & Wheeler, R. 2005. Breeding biology of Masked boobies (Sula dactylatra tasmani) on Lord Howe Island, Australia. Emu 105, 105-113.

Steeves, T. E., Anderson, D. J. & Friesen, V. L. 2005a. A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the masked booby (Sula dactylatra). Molecular Ecology 14, 3877-3887.

- ., Anderson, D. J. & Friesen, V. L. 2005b. The Isthmus of Panama: a major physical barrier to gene flow in a highly mobile pantropical seabird. Journal of Evolutionary Biology 18, 1000-1008.

- ., Anderson, D. J., McNally, H., Kim, M. H. & Friesen, V. L. 2003. Phylogeography of Sula: the role of physical barriers to gene flow in the diversification of tropical seabirds. Journal of Avian Biology 34, 217-223.

Vanderwerf, E. A., Becker, B. L., Eijzenga, J. & Eijzenga, H. 2008. Nazca booby Sula granti and Brewster's brown booby Sula dactylatra brewsteri in the Hawaiian Islands and Johnston and Palmyra atolls. Marine Ornithology 36, 67-71.

Van Tets, G. F., Meredith, C. W., Fullagar, P. J. & Davidson, P. M. 1988. Osteological differences between Sula and Morus, and a description of an extinct new species of Sula from Lord Howe and Norfolk Islands, Tasman Sea. Notornis 35, 35-57.