Dodo

dodo_scenery_julian-hume_nowatermarked
The biota in lowland Mauritius. Julian Hume; http://www.julianhume.co.uk

As stated by David Quammen, “the story of the dodo is obscured by a fog of uncertainties.” By about 1690, if not earlier, it was extinct in its area of endemism, Mauritius. Starting around 1500 with the arrival of Europeans, Mauritius, Rodrigues, and Réunion in the Indian Ocean lost 33 species of birds, including the dodo, 30 species of land snails, and 11 reptiles.

Dodo, Raphus cucullatus
Dodo, Raphus cucullatus, Attr. Roelandt Savery, ca. 1626. This oil on canvas is a most famous paintig of the dodo attributed to the Flemish painter, R. Savery. Taking this painting as a guide, Richard Owen placed the bones arranging them over it to get the first scientific description of the fossil remains, published in 1866. Natural History Museum, London, UK.

 

As other large pigeons, especially on islands, dodos probably relied extensively on fruit food. A famous iconic story relates the extinction of dodos, to the almost co-extinction of a seemingly preferred fruiting tree, Sideroxylon grandifolium (formerly Calvaria major, Sapotaceae, the tambalacoque tree), thought to have relied exclusively on these birds for seed dispersal. The tree is an endemic species. According to historical records, it had once been common in upland Mauritian forests and was often exploited for lumber. According to the original hypothesis of coextinction, set by Temple (1977) based on a traditional belief of Mauritius people: “In response to intense exploitation of its fruits by dodos, S. grandifolium evolved an extremely thick endocarp as a protection for its seeds; seeds surrounded by thin-walled pits would have been destroyed in the dodo’s gizzard. These specialized, thick-walled pits could withstand ingestion by dodos, but the seeds within were unable to germinate without first being abraded and scarified in the gizzard of a dodo.

Dodos were large-bodied birds, averaging- according to the most recent estimates- 10 kg and reaching up to 12 kg (previous estimates reported up to ~21 kg). The beak was very robust, ~5 cm gape width, probably apt to handle and swallow very large fruits as well as other plant material.

Dodo XVII century drawings
Seventeenth century depictions of Raphus cucullatus. a, A lean dodo (C. Clusius 1605). b, A fat dodo by A. Van de Venne (1626). Recent mass estimates (Angst et al. 2011) are in better agreement with a than with b, supporting the idea that pictures of extremely fat dodos are exaggerations, not necessarily based on living dodos and often copied from other artists. See Strickland & Melville (1848) for details and additional illustrations.

Coextinctions are extremely difficult to demonstrate, especially for interactions involving, e.g., small species (e.g., ectoparasites and hosts) and species involved in generalized interactions (plant-animal mutualisms for pollination and seed dispersal). Yet we have many evidences for functional coextinctions, happening when species become very rare (even extinct) and their ecological roles are lost. Dodos and tambalacoques probably illustrate this. S. grandifolium has persisted on the island likely because of haphazard dispersal by other dispersal agents (e.g., giant skinks and turtles) and rare instances of runoff, etc. Seeds have been found germinating in some cases, yet with very low proportions; while pulp removal was required for germination, it appears that seed scarification does not improve germination significantly. And dodos may had the ability to crack the hard seeds during digestion. Yet there is no proper test available about of all these aspects, as far as I know.

Tambalocoque seed
A tambalocoque (Sideroxylon grandiflorum, Sapotaceae) seed.

The tree still remains in relict stands but juveniles can be found. The dispersal has certainly collapsed, yet with no final effect entailing the extinction of the tree on the island. Probably many local stands of S. grandifolium have disappeared since dodo’s extinction ca. 400 yr ago. Recent analyses of rich fossil plant and animal remains in lowland Mauritius include many S. grandifolium seeds associated with dodo and giant turtle remains. But it seems we are not in front of a tightly coevolved one-to-one instance of pairwise coevolution. Most likely, not simply the dodo extinction contributed to the rarity of tamabalacoques on Mauritius (and several other large-seeded trees): competition with exotic species, were most likely fundamental. Introduced species included Javan deer, goat, pig, crab-eating macaque, and black rat were clear contributors for the dodo’s extinction by destroying the understory vegetation, competing for food sources, and, in the case of the pig, macaque, and black rat, direct predation on eggs and chicks.

roland-saverys-figure-of-the-dodo_1626
Fac-simile of Roland Savery’s figure of the Dodo in his picture of the Fall of Adam, in the Royal Gallery at Berlin.

Independently of whether the initial reports of coextinction due to loss of the mutualistic dodo were wrong, or biased, or both, the system reflects what happens when ecological interactions are lost: we simply see highly altered systems that remain extremely difficult- or even impossible- to resurrect. And oftentimes the extinction of interactions precedes by a long time the extinction of species, so that what we see is the pervasive effect of the debt of lost interactions.

  • Angst, D., Buffetaut, E. & Abourachid, A. (2011) The end of the fat dodo? A new mass estimate for Raphus cucullatus. Naturwissenschaften, 98, 233–236.
  • Herhey, D. (2006) The widespread misconception that the tambalacoque or Calvaria tree absolutely required the dodo bird for its seeds to germinate. Plant Science Bulletin, 50, 105–109.
  • Oudemans, A.C. (1917). Dodo-Studien. Johannes Muller, Amsterdam.
  • Pimm, S.L. (2002) The dodo went extinct (and other ecological myths). Annals of the Missouri Botanical Garden, 190–198.
  • Quammen, D. (1996) The Song of the Dodo. Scribner, NY, USA.
  • Rijsdijk, K.F., Hume, J.P., Louw, P.G.B.D., Meijer, H.J.M., Janoo, A., De Boer, et al. (2016) A review of the dodo and its ecosystem: insights from a vertebrate concentration Lagerstätte in Mauritius. Journal of Vertebrate Paleontology, 35, 3–20.
  • Strickland, H.E., Melville, A.G. (1848) Dodo and its kindred. History, affinities, and osteology of the dodo, solitaire, and other extinct birds of the islands Mauritius, Rodriguez, and Bourbon. Reeve, Benham and Reeve, London, UK.
  • Temple, S.A. (1977) Plant-animal mutualism: coevolution with dodo leads to near extinction of plant. Science, 197, 885–886.
  • Witmer, M.C. & Cheke, A.S. (1991) The dodo and the tambalacoque tree: an obligate mutualism reconsidered. Oikos, 61, 133–137.
    Text: Pedro Jordano. Illustrations and photos, from digitized original books at Biodiversity Heritage Library, and Spanish National Library. Also, photos by M. Galetti and P. Jordano.

Ginkgo

Ginkgoes and dodos are my two favorite icons of “ghost” mutualistic interactions. So, I had the two last posts on megafauna and extinct interactions dedicated to them.

There are only five living groups of seed plants, and ginkgo is one of them; just a single species. Ginkgoes (Ginkgo biloba, Ginkgoaceae) have fleshy “fruits” and their “seeds” were dispersed by animals including, most probably, from dinosaurs to Pleistocene megafauna, and to extant frugivores nowadays. The reason is that the ginkgo has survived on Earth for a really extended period of time, with the earliest fossils of ginkgo-like plants dated more than 200 million years ago. Among the many ginkgo-like tree species, only Ginkgo biloba has survived (up to five Ginkgo species are known as fossils).

gbiloba

Living ginkgo very nearly went extinct, in fact, as of two million years ago, existing in only a small area in eastern China, the Tian Mu Shan mountains in Guizhou Province. Ginkgoes have then survived just by human intervention, with an assisted dissemination for cultivation starting at least 1200 yr ago by Buddhist monks, and introduced to Europe just by 1730-1750.

captura-de-pantalla-2016-12-30-a-las-5-51-41-pm
From Engelbert Kaempfer in his Amoenitates, 1712: the first illustration of ginkgo by a Western botanist.

Most likely a combination of extreme dispersal limitation due to lack of efficient seed dispersers combined with large-scale climate shifts and habitat modification contributed to their nearly extinction in the wild. Contrary to other tree species, retractions to small refugia populations failed to recover the original range, especially in North America and Europe. As with other megafauna-dependent species, it resprouts vigorously from buds buried in its underground parts, and human use certainly rescued the ginkgoes, probably because of their nutritous “nut”. In Peter Crane’s words: “It is irrepressible; its capacity for self-preservation has helped it survive through millions of generations.”

We know very little about how seed dispersal works in living ginkgo. The fleshy “fruit” is really the mature, fertilized ovule with a a three-layered integument: a fleshy outer sarcotesta, a stony inner sclerotesta, and a thin endotesta. Its smelly, large seeds (20-30 mm x 16-24 mm) are one of its most well-known and distinctive features: the seed’s soft outer layer starts to break down after a few days on the ground and produces butyric acid, CH3(CH2)2COOH giving it the “interesting” odor. Germination improves after the fleshy seed coat has been removed by passing through the gut of an animal or being teared-off. In one of the potentially wild ginkgo populations in China it is documented that the seeds are eaten by a wild cat, and in Japan they are eaten by badgers. Yet, there were very few seedlings in this population, located in 1989 by Del Tredici, despite good fruiting. People harvested the nuts, which are very nutritious, as well as Pallas’s squirrels (Callosciurus erythraeus), which also may act as good dispersers by scatter-hoarding the seeds.

Yet who were the seed dispersers that mediated the range expansion of ginkgoes over continents and islands (Japan) before human-mediated propagation? As in other megafauna-dependent plants, most likely a combination of dispersal agents, including large and medium-sized mammals and, well before that, dinosaurs. As with other extant large-‘seeded’ Coniferopsida like Cephalotaxus and Torreya with very large seeds, scatter-hoarding animals like the extinct multituberculates (i.e., the ‘rodents’ of the Mesozoic; g. Ptilodus) would have played a role in active seed dispersal of ginkgoes by scatter-hoarding the seeds.

We can see ginkgoes as survivors with a long history of mutualistic interactions involving a diverse array of animals, whose actual diversity we can only speculate about, then replaced by extensive human use.

  • van Beek, T.A. (2003) Ginkgo biloba. CRC Press, NY.
  • Crane, P. (2013). Ginkgo. The tree that time forgot. Yale University Press, New Haven.
  • del Tredici, P. (1989) Ginkgos and multituberculates: evolutionary interactions in the Tertiary. Bio Systems, 22, 327–339.

Text: Pedro Jordano with excerpts from Del Tredici (1989) and Crane (2013). Illustrations: WikiMedia.

Megafauna in Madagascar

pleistocene_madagascar_final_by_wsnyder-d7f6uwm

A scene in Madagascar in the late Pleistocene. From left to right: elephant bird (Aepyornis maximus), Malagasy giant rat (Hypogeomys antimena), melanistic giant fossa (Cryptoprocta spelea), monkey lemur (Archaeolemur), streaked tenrec (Hemicentetes), and koala lemur (Megaladapis).

Madagascar had a highly diversified megafauna, as also occurred in other islands, quickly becoming defaunated because of human action and habitat destruction, starting very recently, ca. 2000 yr BP. For example, the Spiny Thicket Ecoregion (STE) of SW Madagascar was home to numerous giant lemurs and other megafauna, including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores.

Island frugivore faunas are much more phylogenetically diverse than continental ones; their frugivore assemblages are known as disharmonic because a given plant species may depend on distinct sorts of animal seed dispersers (e.g., lizards, birds, mammals) quite distinct in evolutionary history and likely not being complementary in their ecological functions. For example, only one-third of the lemur species which earlier occupied the spiny thicket ecoregion survive today. The extinct lemurs occupied a wide range of niches, often distinct from those filled by non-primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Recent evidence using stable isotope biogeochemistry has shown that most extinct lemurs fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets.
While the negative effects on seed dispersal of Pleistocene megafauna extinction in continental areas were probably buffered by complementary dispersers (e.g., scatter-hoarders, domestic megafauna, human use), island assemblages had not this option. Thus, if we seek instances of actual co-extinction of co-dependent frugivores and their food plants we may probably have to resort to islands, especially oceanic islands, or extreme habitats (e.g., deserts) where the mutualistic partners are highly disharmonic.

  • Crowley, B.E., Godfrey, L.R. & Irwin, M.T. (2011) A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar. American Journal of Primatology, 73, 25–37.
  • Grubb, P.J. (2003) Interpreting some outstanding features of the flora and vegetation of Madagascar. Perspectives in Plant Ecology Evolution and Systematics, 6, 125–146.
  • Jungers, W.L., Demes, B. & Godfrey, L.R. (2007) How big were the “‘giant’” extinct lemurs of madagascar? J. G. Fleagle, C. C. Gilbert (eds.), Elwyn Simons: A Search for Origins. Springer, pp: 1–18.
  • Shapcott, A., Rakotoarinivo, M., Smith, R.J., Lysakova, G., Fay, M.F. & Dransfield, J. (2007) Can we bring Madagascar’s critically endangered palms back from the brink? Genetics, ecology and conservation of the critically endangered palm Beccariophoenix madagascariensis. Botanical Journal of the Linnean Society, 154, 589–608.

Text: Pedro Jordano; excerpts fromCrowley et al. 2011.
Illustration: William Snyder @deviantart.com (Pleistocene Madagascar).

It takes guts to disperse seeds: the amazing physiologies of megafauna

Megafauna can be divided in two large groups in terms of food digestion: foregut and hindgut fermenters, depending on where in the digestive tract the ingesta is digested. Foregut fermenters include ruminants, pseudoruminants (i.e., hippo, camelids), just the hoatzin among birds, and the colobine monkeys, sloths, and some marsupials and rodents- all them have complex, multipart stomachs. Hindgut fermenters are monogastric herbivores.

The very large megafauna are largely non-ruminants and may have either foregut or hindgut fermentation of food, with this having very important consequences for seed treatment. While the largest extant non-ruminant foregut fermenter is the hippopothamus, the largest terrestrial animals nowadays are hindgut fermenters, with the exception of large bovids: elephants, rhinos, equids, tapirs.

Interestingly, the digestive tract of elephants is surprisingly short compared to other herbivorous mammals. Typical retention times of ingesta in elephants are below 50h; with Asian elephants achieving higher digestion coefficients on comparable diets, and having longer ingesta mean retention times, than their African counterparts. This is probably associated to the fact that intestine lengths of Asian elephants (~30m) nearly double those of African elephants (~15m) for a given body mass.

digestive_systems-001
The diversity of digestive systems among several types of mammal hindgut fermenters. a, peccary; b, pig; c, zebra; d, tapir; e, African elephant; f, Asian elephant; g, rhino.

Tapirs, in the order Perissodactyla, are the closest extant relatives to equids and rhinoceroses, thus their digestive tract reportedly resembles that of horses. They both have a large caecum and proximal colon as fermentation chambers. In both the horse and the rhinoceros, the caecum and colon have approximately the same width. In contrast, the tapir also has a large caecum, but the rest of the large intestine—in particular, the ventral proximal colon— is less voluminous. The caecum of the tapir is its most voluminous gastro-intestinal section, suggesting that during the evolutionary history of tapirs, and in contrast to other extant perissodactyls, the caecum was the major fermentation site in the digestive tract.


The caecum of rhinos, horses, and probably also tapirs may retain seeds for many days (kind of a side-storage of indigestible food), being suddenly evacuated in pulses. The browsing black rhinoceros (Diceros bicornis) has both shorter small and large intestines than the grazing rhinoceroses (Ceratotherium simum, Rhinoceros unicornis).

Peccaries in contrast, are foregut fermenters, with a digestive tract characterised by an elaborate forestomach. Peccaries have a small relative stomach volume compared to other foregut fermenters, which implies a comparatively lower fermentative capacity and thus forage digestibility. The forestomach could enable peccaries to deal, in conjunction with their large parotis glands, with certain plant toxins (e.g. oxalic acid).

This fascinating diversity of digestive strategies and food processing has undoubtely emerged from coevolved interactions with plants, either as antagonistic herbivores or mutualistic seed dispersers. Plants were benefited by megafauna evolving very large body sizes (especially among monogastric hindgut fermenters), yet with relatively short retention times that did not damage seeds, even with a lengthy digestion process; however, with more limitations to detoxify plant toxins compared to ruminants. Many of the extremely large extinct megafauna (e.g., Indricotherium, reaching up to 15000 kg body mass) were most likely hindgut fermenters with browsing habits and extensive use of fruit food. Ruminants, on the other hand, have been likely limited in their evolution to smaller body sizes (up to 1200 kg in some bovids, 2700 kg in hippos). All the very large ruminants (bovids, buffalo, zebu), but not the smaller ones (e.g., antelopes) lack the ability to reabsorb water in the colon and depend on the availability of drinking water.

The combinations of digestive characteristics of monogastric hindgut fermenters supports their key ecologial functions for seed dispersal: 1) ample diversity of plant food species dispersed; 2) extremely large number of seeds dispersed due to huge gut capacities; 3) long seed dispersal distances due to long retention times with a distinct role of caeca; and 4) gentle treatment to seeds during mastication and digestion, favouring adequate germination potential of dispersed seeds in most instances.

Photos: Kulpat Saralamba, Kim McKonkey, Mauro Galetti, Carlos R Brocardo, WikiCommons.

  • Clauss, M. & Hummel, J. (2005) The digestive performance of mammalian herbivores: why big may not be that much better. Mammal Review, 35, 174–187.
  • Clauss, M., Steinmetz, H., Eulenberger, U., Ossent, P., Zingg, R., Hummel, J. & Hatt, J.M. (2006) Observations on the length of the intestinal tract of African Loxodonta africana (Blumenbach 1797) and Asian elephants Elephas maximus (Linné 1735). European Journal of Wildlife Research, 53, 68–72.
  • Clauss M, Steuer P, Müller DWH, Codron D, Hummel J (2013) Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism. PLoS One 8:e68714
  • Hagen, K., Müller, D.W.H., Wibbelt, G., Ochs, A., Hatt, J.-M. & Clauss, M. (2014) The macroscopic intestinal anatomy of a lowland tapir (Tapirus terrestris). European Journal of Wildlife Research, 61, 171–176.
  • Müller, D.W.H., Codron, D., Meloro, C., Munn, A., Schwarm, A., HUMMEL, J. & Clauss, M. (2013) Assessing the Jarman–Bell Principle: Scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores. Comparative Biochemistry and Physiology, Part A, 164, 129–140.
  • Schwarm, A., Ortmann, S., Rietschel, W., Kühne, R., Wibbelt, G. & Clauss, M. (2009) Function, size and form of the gastrointestinal tract of the collared Pecari tajacu (Linnaeus 1758) and white-lipped peccary Tayassu pecari (Link 1795). European Journal of Wildlife Research, 56, 569–576.

Moas

The diversity of moas was extraordinary, including nine (10, for some authors) species in six different genera, all them endemic to New Zealand. They nicely illustrate megafaunal birds, whose extant furgivorous relatives include cassowaries and, with partial frugivory, kiwis.

Moas weighted 35-250 kg, becoming extinct ~1300-1440 yr BP due to overhunting. Moas included at least three distinct assemblages in the South Island during the Holocene: a wet western beech forest assemblage consisting of South Island giant (Dinornis robustus) and little bush (Anomalopteryx didiformis) moas; an assemblage from the relatively dry eastern forests and scrublands, consisting of South Island giant, eastern (Emeus crassus), heavy-footed (Pachyornis elephantopus) and stout-legged (Euryapteryx gravis) moas; and an assemblage from upland and subalpine areas consisting of South Island giant, crested (Pachyornis australis) and upland (Megalapteryx didinus) moas.

The discovery in New Zealand of Late Holocene deposits of coprolites from these extinct avian megaherbivores has provided a unique opportunity to gain a detailed insight into the ecology of these birds across ecologically diverse habitats. Macrofossil analysis of 116 coprolites of the giant ratite moa (Aves, Dinornithiformes) reveals a diverse diet of herbs and low shrubs in both semi-arid and high rainfall ecological zones, overturning previous models of moa as dominantly browsers of trees and shrubs.
Ancient DNA analysis identified coprolites from four moa species (South Island giant moa, Dinornis robustus; upland moa, Megalapteryx didinus; heavy-footed moa, Pachyornis elephantopus and stout-legged moa, Euryapteryx gravis), revealing a larger dietary variation between habitat types than between species. Most species of moa, if not all, included fruit in their diets, and may have been also important as dispersers of grass seeds.

The new data confirm that moa fed on a variety of endemic plant taxa with unusual growth forms previously suggested to have co-evolved with moa. Lastly, the feeding ecologies of moa are shown to be widely different to introduced mammalian herbivores. The broad range of feeding strategies used by moa, as inferred from interspecific differences in biomechanical performance of the skull, provides insight into mechanisms that facilitated high diversities of these avian megaherbivores in prehistoric New Zealand.

  • Atkinson, I.A.E. & Greenwood, R.M. (1989) Relationships between moas and plants. New Zealand Journal of Ecology, 12, 67–96.
  • Attard, M.R.G., Wilson, L.A.B., Worthy, T.H., Scofield, P., Johnston, P., Parr, W.C.H. & Wroe, S. (2016) Moa diet fits the bill: virtual reconstruction incorporating mummified remains and prediction of biomechanical performance in avian giants. Proceedings of the Royal Society of London Series B-Biological Sciences, 283, 20152043–9.
  • Bond, W., Lee, W. & Craine, J. (2004) Plant structural defences against browsing birds: a legacy of New Zealand’s extinct moas. Oikos, 104, 500–508.
  • Burrows, C.J., McCulloch, B. & Trotter, M.M. (1981) The diet of moas based on gizzard contents samples from Pyramid Valley, North Canterbury, and Scaife’s Lagoon, Lake Wanaka, Otago. Records of the Canterbury Museum, 9, 309–336.
  • Lee, W.G., Wood, J.R. & Rogers, G.M. (2010) Legacy of avian-dominated plant-herbivore systems in New Zealand. New Zealand Journal of Ecology, 34, 1–20.
  • Wood, J.R., Rawlence, N.J., Rogers, G.M., Austin, J.J., Worthy, T.H. & Cooper, A. (2008) Coprolite deposits reveal the diet and ecology of the extinct New Zealand megaherbivore moa (Aves, Dinornithiformes). Quaternary Science Reviews, 27, 2593–2602.
  • Wood, J.R., Wilmshurst, J.M., Richardson, S.J., Rawlence, N.J., Wagstaff, S.J., Worthy, T.H. & Cooper, A. (2013) Resolving lost herbivore community structure using coprolites of four sympatric moa species (Aves: Dinornithiformes). Proceedings of the National Academy of Sciences USA, 110, 16910–16915.

The Gardeners of the Forest

Elephants are the major gardeners of the rainforest. Weighing around 4000 kg, they are more than twice as large as the next biggest sympatric animal species (the one-horned rhinoceros) and four times as large as the third-place finisher (the gaur, Bos gaurus). Current taxonomy recognizes two extant species of elephant, the African elephant (Loxodonta africana), with forest and savannah subspecies, and the Asian elephant (Elephas maximus). They disperse massive amounts of seeds in conditions adequate for germination and establishment of tree seedlings, with estimates ranging between 300-2000 seeds/km2/day depending on elephant species and habitat. Recent studies indicate that seeds taken from elephant dung germinated as well or better than seeds from bovid dung or directly from fruit. Elephants were calculated to move seeds up to 10 times as far as domestic bovids. When elephants are missing, there are no ecological counterparts to compensate their absence.


The video from the Elephant Reintroduction Foundation nicely cartoons the type of mechanistic models that help us to estimate the ecological functions derived from mutualistic interactions between these megafrugivores and plants.
An empirical probability model estimated that the loss of elephants would result in reductions of about 66%, 42%, and 26% in the number of successfully dispersed seeds of key species such as Dillenia indica (chalta), Careya arborea (kumbhi), and Artocarpus chaplasha (lator), without compensation. In compensation scenarios, other frugivores could ameliorate reductions in dispersal, making them as low as 6% if species such as gaur (Bos gaurus) persist. Thus the importance of elephants as seed dispersers is amplified by the population reductions of other large disperser species throughout tropical Asia. The African and Asian elephants are the exclusive or near-exclusive disperser of a considerable number of plant species. The loss of forest elephants (and other large-bodied dispersers) may lead to a wave of recruitment failure among animal-dispersed tree species, and favor regeneration of the species-poor abiotically dispersed guild of trees.

– Beaune, D., Fruth, B., Bollache, L., Hohmann, G. & Bretagnolle, F. (2013). Doom of the elephant-dependent trees in a Congo tropical forest. Forest Ecology and Management, 295, 109–117.
– Blake, S., Deem, S.L., Mossimbo, E., Maisels, F. & Walsh, P. (2009) Forest elephants: tree planters of the Congo. Biotropica, 41, 459–468.
– Campos-Arceiz, A., & Blake, S. (2011). Megagardeners of the forest – the role of elephants in seed dispersal. Acta Oecologica, 37, 542-553.
– Sekar, N., Lee, C.L. & Sukumar, R. (2015). In the elephant’s seed shadow: the prospects of domestic bovids as replacement dispersers of three tropical Asian trees. Ecology, 96, 2093–2105.
– Sukumar, R. (2003). The living elephants: evolutionary ecology, behavior, and conservation. New York: Oxford Univ. Press.

The Cryptic Extinctions

McConkey, K.R. & O’Farrill, G. (2016) Loss of seed dispersal before the loss of seed dispersers. Biological Conservation, 201, 38–49.

Cryptic function loss is a loss in the function of a species that is hidden by its continued presence in the ecosystem; the species may still be present and showing up in a biodiversity inventory, yet its functional ecological role has disappeared. 
The authors reviewed the evidence for cryptic function loss to be widespread among seed disperser populations that persist under disturbed conditions. The results overwhelming support for the seed dispersal effectiveness of animals to be negatively impacted by all forms of disturbance (population decline, changes in community assemblages, habitat change, and climate change). However, seed dispersal was positively affected in some examples, particularly when extirpation of an interacting frugivore or predator enhanced fruit consumption. 

gaur3
A group of gaurs (Bos gaurus) (also known as Indian bison); a species listed as vulnerable on the IUCN Red List since 1986. The population decline in parts of the species’ range is likely to be well over 70% during the last three generations. Photo: Kulpat Saralamba.

Behavioral changes are usually the first adaptation of an animal to disturbance and are likely to be a common trigger for function loss without species loss, resulting in the animal no longer performing a function carried out previously. Substantial decrease in population density or demography of an animal species can also trigger cryptic function loss; for example, when specialization occurs among individuals within a single population and a non-random subset of individuals is particularly vulnerable to a disturbance. Finally, cryptic function loss can occur through phenotypic adaptation of an animal species, when the physical alteration enhances survival but is not matched by interacting species.
Given the ample generalization shown by many seed dispersal systems, we are far from understanding the consequences of functional losses due to population density collapses of frugivore species triggered by disturbances. In Dan Janzen’s words, this is the most pervasive kind of extinction, the extinction of interactions.

See also:
– Jarić, I., 2015. Complexity and insidiousness of cryptic function loss mechanisms. Trends in Ecology and Evolution 30, 371–372.
– Valiente-Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci, A., Galetti, M., García, M.B., García, D., Gomez, J.M., Jordano, P., Medel, R., Navarro, L., Obeso, J.R., Oviedo, R., Ramírez, N., Rey, P.J., Traveset, A., Verdú, M., Zamora, R., 2015. Beyond species loss: the extinction of ecological interactions in a changing world. Functional Ecology 29, 299–307.

Text: Excerpts from McConkey, K.R. & O’Farrill, G. 2016; and Pedro Jordano. Photo: Kulpat Saralamba.