It needs to be better appreciated that the vast majority of modern ecosystems and communities are ‘broken’ or, at least, very much incomplete compared to the situation present within very recent geological history: they lack an often significant number of key component species including some, many or all of the so-called keystone species. Why? As is well known, human hunting, climatic change and a combination of the two has eradicated a diverse assemblage of big-bodied mammals, birds, crocodylians, tortoises and other taxa across the Americas, Australasia, the Pacific and elsewhere. Small-bodied taxa have been removed as well, across the board.

The animals I have in mind were generally ubiquitous throughout the Pleistocene, persisted into the early parts of the Holocene (that is, the last 11,700 years or so) and, in cases, survived into truly ‘modern’ times. Gigantic herbivorous birds, like moa on New Zealand and elephant birds on Madagascar, for example, were still alive as recently as 1000 years ago (at least). Even in places where the megafauna has persisted (many of the Eurasian and east African taxa are still extant, for example), they are substantially reduced in population and range, typically being extinct across huge tracts of their historical range. The end (read: modern) result of this wave of extinctions is a set of depauperate communities where whole setups, entire ecosystems, are missing some, many or all of the parts they co-evolved with (Johnson 2009). Plants produce specialised seeds and fruits for animals that are no longer around to exploit and transport them, and prey species exhibit defences for predators that no longer hunt them, or are super-abundant and have caused partial or total ecosystem collapse due to a knock-on effect that has initiated a so-called trophic cascade (Eisenberg 2010).

This idea – that the ‘ghosts’ of lost species can be detected in extant ecosystems – essentially arose in the 1970s as ecologists began to consider the impact that giant, recently extinct herbivores (specifically, moa on New Zealand) must have had on local floras. The idea became increasingly popular to the extent that people began to report ‘ghosts’ everywhere. On the one hand, it might be true that co-evolution with mostly lost megaherbivores is common and perhaps ubiquitous, given the state the world is in. On the other hand, it can be all too easy to jump to conclusions about perceptions of co-evolution and we often need to consider other possibilities: plants may grow tall, may grow weird or giant fruit, or may exhibit ‘defensive’ adaptations for reasons unrelated to the presence of their predators, for example, since plants have complex evolutionary interactions all their own. Indeed, some classic alleged examples of co-evolution that supposedly involve lost partners are now thought to be erroneous (see the section below on Dodos and Tambalacoque trees).

In the remainder of this article, I want to talk specifically about pieces of evidence that – so it’s been suggested – represent the leftovers of co-evolutionary relationships that specifically involve birds. Don’t get me wrong – there are ‘incomplete’ modern relationships that involved tortoises, mammals and other animals too (see Barlow (2000) and Johnson (2009) for reviews) – but I’ll have to cover them some other time (yeah yeah, sure).

And we’ll start with New Zealand, since it’s the plants and animals here that – together with tropical American fruits that look suited for absent proboscideans (Janzen & Martin 1982) – really kick-started the idea of these ‘biological ghosts’.

Anti-moa browsing adaptations…. or not

Many plants endemic to New Zealand are spiny, appear morphologically similar to toxic species, resemble dead twigs, have purplish-black or dark bronze ‘camouflaged’ juveniles, or possess a so-called divaricating morphology where the branches are tough and wire-like, diverge at high angles, and form a ‘cage’ around the small, widely spaced leaves (Atkinson & Greenwood 1989, Worthy & Holdaway 2002). Greenwood & Atkinson (1977) and other authors interpreted these features as anti-browsing adaptations that co-evolved with moa.

However, the hypothesis that divarication is explained by co-evolution with moa is controversial since it’s been argued that divarication can also represent adaptation to both low air temperatures and to the minimisation of damage caused by either frost or bright sunlight (Howell et al. 2002). Furthermore, moa gizzard contents show that moa clipped twigs from divaricating species and weren’t demonstrably interested in consuming the ‘protected’ foliage anyway (Burrows 1980). Other objections have been raised as well (Worthy & Holdaway 2002). Ergo, it remains controversial as to whether the floral peculiarities seen on New Zealand really do represent anti-moa adaptations or not... maybe they don't.

Burrs for elephant birds, flowers for hummingbirds

A set of branch and foliage characteristics are present in over 20 plant lineages endemic to Madagascar: these features make them wiry and springy and have often been interpreted as anti-browsing adaptations (Bond & Silander 2007). The large prickly fruits of the Madagascan sesame plant Uncarina have been suggested to be trample burrs that were distributed across open habitats by large, terrestrial herbivores (Midgley & Illing 2009) [adjacent image by Didier Descouens]. These floral characteristics almost certainly represent co-evolution with the browsing habits of elephant birds or aepyornithids: we can imagine these giant birds clipping foliage from shrubs and trees (and hence exerting continual pressure on these plants), but also moving across the landscape with great spiky Uncarina burrs stuck to their plumage or skin (ouch). Thorns on Hawaiian lobelias have also been suggested as an anti-browsing adaptation, in this case as a possible defence against the recently extinct moa-nalos (James & Burney 1997), a group of large, flightless waterfowl.

Another, more surprising possible case of bird-plant co-evolution was suggested by Mayr (2005) following the discovery of the stem-hummingbird Eurotrochilus in the Lower Oligocene of Germany. So-called ornithophilous plants in the New World possess features that make them especially attractive to hummingbirds; curiously, several African and Asian plants (including Agapetes, Canarina eminii and Impatiens sakeriana) also look ornithophilous. More specifically, they look suited for co-evolution with hovering avian pollinators, not simply with any old nectarivorous groups, like the sunbirds that pollinate them today (Bartoš et al. 2012). Mayr (2005) suggested that these plants are relicts of co-evolution with extinct Old World hummingbirds [Adjacent hummingbird photo by Charlesjsharp]. If this suggestion is valid, it indicates that Old World hummingbirds fed by sustained hovering in the same manner as extant New World taxa. I would like to know what botanists think of Mayr’s idea – is hummingbird-induced pressure the only likely cause of the ornithophilous morphology?

The sorry case of the Dodo and the Tambalacoque tree

Of all the cases discussed in this article, without doubt the most popular and well known concerns that giant flightless pigeon, the Dodo Raphus cucullatus. The Dodo became extinct some time round about 1690 (give or take a decade or two on either side). During the 1970s, it seemed that an endemic Mauritian tree – the Tambalacoque tree Sideroxylon grandiflorum (formerly Calvaria major) – was down to just its last few specimens, all of which were ailing, centuries-old individuals.

In two much-read articles (both published in Science, no less), Stanley Temple (1977, 1979) explained how modern Tambalacoque seeds never germinated and that the general form of the Tambalacoque’s thick-shelled seeds look suited for co-evolution with a large herbivore. He made the intriguing suggestion that Sideroxylon had evolved a mutualistic relationship with the Dodo, the extinction of the latter now meaning that Sideroxylon was doomed since it relied on the bird for successful germination. This idea is mentioned in Gerald Durrell’s books Golden Bats and Pink Pigeons and I’ve met various people who remember Durrell’s (1977) discussion of it. What they don’t remember is Durrell highly perceptive comment “It’s a lovely story… but I’m afraid it’s got more holes in it than a colander” (Durrell 1977).

Indeed, Temple’s hypothesis of obligate mutualism between the two species has been known not to be true ever since botanists went looking for live Tambalacoque trees and found them, at all growth stages, and with no anachronistic dodos around (Witmer & Cheke 1991). Some Mascarene specialists have referred to Temple’s hypothesis as “notorious” and even as a “myth” (Cheke & Hume 2008).

The ghosts of predators past?

Behavioural and morphological traits present in various extant animals have also been suggested to represent co-evolution with now extinct birds. The cryptic colouration and nocturnal habits of various New Zealand birds, for example, plausibly represent the results of predation pressure previously exerted by extinct raptors (Holdaway 1989, Diamond 1990). The giant New Zealand eagle Hieraeetus moorei (or Harpagornis moorei) appears to have been a formidable predator of other birds and may well have exerted considerable pressure on other species; the large, accipiter-like harrier Circus eylesi was also almost certainly a bird-killer.

However, again we should be sceptical of the idea that extinct raptors are wholly responsible for the possible adaptive responses we have in mind here, since less exotic predators (like skuas and even kea) might also have driven the evolution of the birds concerned.

Meanwhile, the strong fear response that Madagascar’s lemurs have of airborne raptors has also been suggested to represent predation pressure from extinct taxa, most notably the gigantic Stephanoaetus mahery (Goodman et al. 1993, Goodman 1994), a relative of the living Crowned eagle S. coronatus of the African mainland. Again, we can be sceptical of the latter idea, since it seems to assume that S. mahery is the only raptor that might represent a possible lemur predator. In fact, we now know that extant Madagascan raptors – including Henst’s goshawk Accipiter henstii and Madagascar Harrierhhawk Polyboroides radiatus – are significant predators of lemurs, even of big species like avahis and ruffed lemurs. Nevertheless, raptors almost certainly exerted far more predation pressure on lemurs in the recent past than they do today: S. mahery was presumably hunting Madagascan primates on a regular basis.

As should be clear from this brief review, there are reasonable indications that the ecological ‘ghosts’ of extinct birds do indeed exist in some modern ecosystems, and doubtless there are other possible examples out there. As should also be clear, we need to be careful not to jump to conclusions when confronted with what look like co-evolutionary features - it’s very easy to see weird floral adaptations and immediately conclude that they owe their form to co-evolution with megafauna. I’m concerned that this has already happened to a degree, and for that reason the zoologists and palaeontologists who look at these floral adaptations really need to talk a lot with botanists, climatologists and ecologists.

Finally, as a Mesozoic-flavoured palaeozoologist I simply have to mention the idea that there might be entire legions of co-evolutionary floral adaptations that remain unknown or unappreciated: did the browsing behaviour of such megaherbivores of the past as sauropods, duckbilled dinosaurs and giant kangaroos result in weird and wonderful plant forms, some of which persist today? It’s something to think about… [image below from here on Antediluvian Salad]

For more on various of the topics mentioned here, see...

Refs - -

Atkinson, I. A. E. & Greenwood, R. M. 1989. Relationships between moas and plants. New Zealand Journal of Ecology 12, 67-96.

Barlow, C. C. 2000. The Ghosts of Evolution: Nonsensical Fruit, Missing Partners, and Other Ecological Anachronisms. Basic Books, New York.

Bartoš, M., Janeček, Š., Padyšáková, E., Patácová, E., Altman, J., Pešata, M., Kantorová, J. & Tropek, R. 2012. Nectar properties of the sunbird-pollinated plant Impatiens sakeriana: a comparison with six other co-flowering species. South African Journal of Botany 78, 63-74.

Bond, W. J. & Silander, J. A. 2007. Springs and wire plants: anachronistic defences against Madagascar’s extinct elephant birds. Proceedings of the Royal Society B 274, 1985-1992.

Burrows, C. J. 1980. Some empirical information concerning the diet of moas. New Zealand Journal of Ecology 3, 125-130.

Cheke, A. & Hume, J. 2008. Lost Land of the Dodo. Yale University Press, New Haven and London.

Diamond, J. M. 1990. Biological effects of ghosts. Nature 345, 769-770.

Durrell, G. 1977. Golden Bats and Pink Pigeons. Collins, London.

Eisenberg, C. 2010. The Wolf’s Tooth: Keystone Predators, Trophic Cascades and Biodiversity. Island Press, Washington.

Goodman, S. M. 1994. Description of a new species of subfossil eagle from Madagascar: Stephanoaetus (Aves: Falconiformes) from the deposits of Ampasambazimba. Proceedings of the Biological Society of Washington 107, 421-428.

Goodman, S. M., O’Connor, S. & Langrand, O. 1993. A review of predation on lemurs: implications for the evolution of social behaviour in small, nocturnal primates. In Lemur Social Systems and their Ecological Basis: 51-66. Kappeler, P. M. & Ganzhorn, J. U. (Eds). New York: Plenum Press.

Greenwood, R. M. & Atkinson, I. A. E. 1977. Evolution of the divaricating plants in New Zealand in relation to moa browsing. Proc. New Zeal. Ecol. Soc. 24, 21-33.

Holdaway, R. N. 1989. New Zealand’s pre-human avifauna and its vulnearability. New Zealand Journal of Ecology 12 (Supplement), 11–25.

Howell, C. J., Kelly, D. & Turnbull, M. T. H. 2002. Moa ghosts exorcised? New Zealand’s divaricate shrubs avoid photoinhibition. Functional Ecology 16, 232-240.

James, H. F. & Burney, D. A. 1997. The diet and ecology of Hawaii’s extinct flightless waterfowl: evidence from coprolites. Biological Journal of the Linnean Society 62, 279-297.

Janzen, D. H. & Martin, P. S. 1982. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215, 19-27.

Johnson, C. N. 2009. Ecological consequences of Late Quaternary extinctions of megafauna. Proceedings of the Royal Society B 276, 2509-2519.

Mayr, G. 2005. Fossil hummingbirds in the Old World. Biologist 52, 12-16.

Midgley, J. J. & Illing, N. 2009. Were Malagasy Uncarina fruits dispersed by the extinct elephant bird? South African Journal of Science 105, 467-469.

Temple, S. A. 1977. Plant-animal mutualism: coevolution with dodo leads to near extinction of plant. Science 197, 885-886.

- . 1979. The dodo and the tambalacoque tree. Science 203, 1364.

Witmer, M. C. & A. S. Cheke. 1991. The dodo and the tambalacoque tree: an obligate mutualism reconsidered. Oikos 61, 133-137.

Worthy, T.H. & Holdaway, R.N. 2002. The Lost World of the Moa. Bloomington: Indiana University Press.