Dodo

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, 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.”

Dodo, Raphus cucullatus -Museum fur Naturkunde, Berlin, Germany .

Strickland & Melville (1848) Plate I. View of the dodo head, Oxford University specimen.

Strickland & Melville (1848) Plate III.

Strickland & Melville (1848) Plate VI.

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.

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.

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.

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.

Megafauna in Madagascar

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.

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.

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. 

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.

Seed dispersal by megafauna (extinct and extant)

I’ll be posting a series on megafauna (extinct and extant) and megafauna-dependent plants that I’ve been contributing to our Facebook page Frugivores & Seed Dispersal during the month of December. The posts focused on megafauna frugivores and megafauna-dependent fruits and seeds, and the processes of dispersal associated with them. I also included other interesting posts on frugivory and seed dispersal, as ever, but megafauna was the focus. Hopefully we contribute to a better appreciation of the distinct ecological roles and the contribution of megafauna species to the functioning and maintenance of ecosystems around the world, specifically on their role as frugivores and seed dispersers.

Among the most spectacular frugivores and seed dispersers we find the Megafauna species, those amazing beasts that impress every naturalist because of their adaptations, life histories, and specific traits. Yet megafauna species are being particularly hard hit by human-driven activities, notably hunting and deforestation. Megafauna species are traditionally defined as being above 40 kg body mass (i.e., > 100 lb), and include a full range of mammals (e.g., rhino, elephants, a number of antelopes, large primates), birds (e.g., ostrich, cassowary, emu), and reptiles (e.g., varanids, turtles). Moreover, think about the late Pleistocene (~12 Kyr BP) extinction of an even richest diversity of megafauna species: toxodons, terrestrial sloths, mamuths, gliptodons, gomphoteres, etc. The study of frugivory and seed dispersal (FSD) by megafauna opens a number of extremely interesting questions, ranging from the role of past history in shaping fruit traits, the lasting signatures of past extinctions of major seed dispersers for plants (e.g., in the genetic pools), the conflicts and interactions with humans in natural and seminatural habitats, the role of extremely long-distance seed dispersal by megafauna and its collapse following extinction, etc.

Illustration: Dadi, “Cada um”.

 

How do furgivorous birds build-up their fruit meals?

This is the third part of a trilogy of papers dedicated to understanding the evolution of fruit colors and visual signals evolved by plants to attract animal mutualists. The paper is now available online at the Proceedings of the Royal Society, Biology website.

Theory predicts that trade among mutualists requires high reliability. Here, we show that moderate reliability already allows mutualists to optimize their rewards. The colours of Mediterranean fleshy-fruits indicate lipid rewards (but not other nutrients) to avian seed dispersers on regional and local scales. On the regional scale, fruits with high lipid content were significantly darker and less chromatic than congeners with lower lipid content.

On the local scale, two warbler species (Sylvia atricapilla and Sylvia borin, above) selected fruit colours that were less chromatic, and thereby maximized their intake of lipids—a critical resource during migration and wintering.

Figure. The trade of resources characterizing mutualistic interactions leads to multiple, repeated interactions among individual producers and consumers. For example, birds use visual information to decide which fruits to consume. Two individual birds combine different fruit species in their meals during a short feeding bout (t0 − t1), along their foraging sequence, in which they visited different fruiting plants. M1–M4 indicate the composition of four meals, i.e. the number of fruits consumed and their species identity, different fruits with different colours. We analyzed the combination of colors in field-sampled fruit meals in relation to the nutrient composition and food “reward” obtained by the birds. Birds used markedly non-random combinations of colors in their meals, indicating a significant choice of fruit meals maximizing energy intake.

In a passage and wintering area in SW Spain where I intensively studied these birds, the two warbler species consistently selected fruit color combinations that were significantly less chromatic, evidencing the use of color as a cue of nutrient rewards during short feeding bouts. Being extremely dependent on fleshy fruits during migration and wintering, these warblers use a very diverse set of fruit species to build-up reserves required for long-distance flights (garden warbler) or winter survival (blackcap).

It is amazing how selective were these birds in their choice of fruits. Even in a short feeding bout blackcaps can ingest up to seven different fruit species. I used analyses of fecal pellets, identifying not only seeds, but also fruit skins in the remains using a microscope, which enabled me to identify the number of different fruit species consumed during a short feeding bout. The fruit meals thus combine a varied assortment of flavors, pulp types, etc. The warblers have a very short gut passage time (16 moon on average- and up to 40 min), so that a sample of faecal material indicates the previous choices of fruits made by the bird, immediately before capture. I used mist-netted birds that were released after capture.

Warblers need to maintain a high throughput of fruits when relying on fruit food because fleshy fruits are a quite “diluted” type of food: not only they are rich in water, quite succulent, but they also have indigestible seeds that occupy very valuable space within the bird’s gut. The birds need to process all this stuff very rapidly in order to get enough “reward”. In turn this is good for the plant because the seeds are readily dispersed away from the mother plant. This is a mutualistic interaction driven by the visual cues used by the birds.

Our results indicate that mutualisms require only that any association between the quality and sensory aspects of signallers is learned through multiple, repeated interactions. Because these conditions are often fulfilled, also in social communication systems, we contend that selection on reliability is less intense than hitherto assumed. This may contribute to explaining the extraordinary diversity of signals, including that of plant reproductive displays.

Now the California gull, Larus californicus

This is the California gull, Larus californicus (Lawrence, 1854). It is subs. californicus.

Here we see the white mirrors in P9 and P10, which are characteristic, and the white trailing edge to inner wing. This (both photos of same individual) is an adult (at least 4cy) with the winter plumage (hindneck has dense brown streaks). These first three photos were taken at Wilder Ranch State Park, Santa Cruz, along the coast line.

A detail of the wonderful head of this gull (same individual in these two photos, an ad). Note the dark iris, and the color pattern in the bill ring (black with red-orange tinted patch in the lower mandible). The bill is characteristically 4-colored: yellowish at the base, black ring, red-orange dot and ivory tip- this separates it from Ring-billed and Herring. The leg color is also characteristic (green-bluish) but apparently is very variable. I saw other ad birds with very yellow legs. These two photos were taken in San Lorenzo Park, Santa Cruz, CA.

This is a 3cy bird, finishing molt to 3rd winter. The bill ring is wholly black; there are no white patches on P feathers, nor white mirrors. The bill is longer than in Ring-billed and the head is more massive. The photo was taken at Moss Landing, Elkhorn Slough, CA.

This is a 1cy bird (juvenile molting into 1st winter plumage), with characteristic black-tipped bill with pale pink in the base. It has not yet started te molt of the scapulars, yet some grayish ones seem to be apparent- the median coverts look worn and faded, creating pale midwing-panel; so the bird is a bit delayed in its molt.

EXIF data:

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Heermann’s gull in my recent trip to California

These are some shots of my recent trip to California, last October, where I had the opportunity to do a whale watching trip offshore Monterrey Bay, from Moss Landing. I’ll be posting more photos soon…

Heermann’s (Larus heermanni (Cassin, 1852) is one of my favorite gulls, with a beautiful plain grey plumage in the adult, contrasting with the white patches and the coral-red bill, and a smooth dark brown plumage of the immature birds.  They were common birds along the coast up to Santa Cruz, quite often in large flocks. The population size is estimated in ca. 150000 pairs.

The adult birds here seem to be starting with the winter plumage, with paler grey heads.

This is a  typical juvenile bird facing its 1st winter. The head is very dark grey, with a creamy base of the bill.

I like the broad white trailing edge of the wing. It’s a very elegant gull in flight (well, as all the gulls). I’m getting a gull-addicted, even for the commonest species, which pose very nice identification problems when you try to get to the details of the plumage patterns and molt. Even the most common species (i.e., the yellow-legged here in S Spain) pose amazing identification challenges, especially in winter.

And here, with the Humpback whale…

The photos were taken with the Nikon D7000, AF-S VR Zoom-Nikkor 70-300mm f/4.5-5.6G IF-ED, f8, 1/1000, ISO 400.

Collared pratincoles

These are several shots of Collared pratincoles (Glareola pratincola, Glareolidae) that I took last weekend, at Marismas de Barbate, Cádiz. It was a very nice day, cloudy, but I was lucky to get close to the birds, creeping a lot. These birds are really beautiful. The geographic distribution is very patchy in the Western Palaearctic, with few areas in the Iberian Peninsula. 

Our study on functional extinction of frugivores, published in Science

Our new paper “Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size”, just published in this week issue of Science.

Mauro Galetti, Roger Guevara, Marina C. Côrtes, Rodrigo Fadini, Sandro Von Matter, Abraão B. Leite, Fábio Labecca, Thiago Ribeiro, Carolina S. Carvalho, Rosane G. Collevatti, Mathias M. Pires, Paulo R. Guimarães Jr., Pedro H. Brancalion, Milton C. Ribeiro, and Pedro Jordano. 2013. Functional Extinction of Birds Drives Rapid Evolutionary Changes in Seed Size. Science 340: 1086-1090.
DOI: 10.1126/science.1233774.

Photos, from top left, descending, to right:

1. Selenidera maculisrotris (male) handling a palmito seed.
2. Palmito fruits with beak marks, dropped beneath the palm, and regurgitated seeds.
3. Turdus flavipes trying to swallow a palmito fruit.
4. Ramphastos vitellinus (subsp. vitellinus) handling a fruit.
5. Selinedera maculirostris (male) picking a fruit.
6. Palmito seedling just after germination (note the seed still attached).
7. Palmito juçara, Euterpe edulis (Arecaceae).
8. Aburria (Pipile) jacutinga.
9. Baillonius (Pteroglossus) bailloni handling a fruit.
10. Turdus amaurochalinus (young), picking a fruit.
11. View of the ompbrphilous atlantic rainfrorest (Mata Atlántica) understory in Carlos Botelho park.
12. Penelope obscura.
13. Pyroderus scutatus, swallowing a fruit.
Photos by: Edson Endrigo, Pedro Jordano, Mauro Galetti, Marina Cortes, Guto Balieiro, and Lindolfo Souto.

The selective extinction of large frugivorous birds is associated with the rapid evolutionary reduction of seed size in a keystone palm.

Local extinctions have cascading effects on ecosystem functions, yet little is known about the potential for the rapid evolutionary change of species in human-modified scenarios. We show that the functional extinction of large-gape seed dispersers in the Brazilian Atlantic forest is associated with the consistent reduction of seed size of a keystone palm species. Among 22 palm populations, areas deprived of large avian frugivores for several decades present smaller seeds than non-defaunated forests, with negative consequences for palm regeneration. Coalescence and phenotypic selection models indicate that seed size reduction most likely occurred within the last 100 years, associated with human-driven fragmentation. The fast-paced defaunation of large vertebrates is most likely causing unprecedented changes in the evolutionary trajectories and community composition of tropical forests.

When we talk about biodiversity we normally refer to the number of species found in a given area. But these species have ecological functions that are essential to the functioning of ecosystems. The loss of a species also entails the loss of the ecological role it plays in the ecosystem, and this kind of extinction happens much unnoticed. We have documented the effect of functional extinction of large fruit-eating birds on an important plant trait – seed size – of a key plant species of the Atlantic Rainforest in Brazil, one of the biodiversity “hot-spots” on the planet. Our study is a natural experiment that takes advantage of the presence of fragmented areas of forest that have remained so since the early 1800s, when the development of crops such as coffee and sugar cane triggered the extensive deforestation of the Atlantic rainforest. Only 12% of the original forest persists, and over 80% of what remains are fragments are too small to maintain large animals. Our results show that the loss of large fruit-eating birds such as toucans leads to the size reduction of the seeds of a palm tree, which is a key species in these Atlantic forests. These evolutionary changes in fruit and seed size have occurred only in defaunated forests, where only small frugivorous birds persist. These small birds only successfully disperse smaller seeds.

We studied 22 populations of this palm tree along the SE coast of Brazil. In the defaunated areas, which persist as fragments from several decades ago, the seed sizes are consistently smaller than in well-preserved forests, and this has negative consequences for regeneration. The smaller seed size in defaunated areas is not explained by other environmental or geographic variables. Fast natural selection: Small birds such as thrushes cannot swallow and disperse large seeds. Large birds, such as aracaris and toucans, play an important role in dispersing seeds of plants, especially of large seeds. In rainforests without toucans large seeds tend to disappear over time because undispersed seeds are attacked by seed predators. Small seeds are more vulnerable to desiccation and cannot withstand projected climate change.

We have combined a number of techniques including field work, genetic analyses, evolutionary models and statistical analyses. We collected ground data on a large number of palm trees in 22 populations, by collecting fruits, observing the avian frugivore assemblage and conducting germination experiments. We have also used DNA genetic markers to employ quantitative genetic models to estimate the intensity of selection on seed traits and coalescence theoretical models to infer the time of isolation of populations. Finally, we statistically analyzed the effect of different types of data, including climatic and environmental information, on seed size variation. 

Our work provides one of the few existing evidence that evolutionary change in natural populations can happen very fast as a direct result of changes induced by human action. The extinction of large vertebrates is happening all over the world and the implication is poorly known. These large bodied species maintain mutualistic interactions with plants: while flesh-fruited plants offer fruits as food sources, frugivores disperse their seeds. Such ecological process ensures natural regeneration of the forest. Unfortunately, the effect we document in our work is probably not an isolated case. The constant extirpation of large vertebrate in natural habitats is very likely causing unprecedented changes in evolutionary trajectories of many tropical species.

Habitat loss and species extinction is causing drastic changes in the composition and structure of ecosystems. This involves the loss of key ecosystem functions that can determine evolutionary changes much faster than we anticipated. Our work highlights the importance of identifying these key functions to quickly diagnose functional collapse of ecosystems.

Components of pollination effectiveness and their consequences in insular pollinator assemblages

Our paper “Quantity and quality components of effectiveness in insular pollinator assemblages” online in Oecologia. Thanks Cande and Alfredo. This is a field study of the pollination of Isoplexis canariensis by birds and lizards in the Canary Islands, a part of Cande Rodríguez PhD project.

Ecologically isolated habitats (e.g., oceanic islands) favor the appearance of small assemblages of pollinators, generally characterized by highly contrasted life modes (e.g., birds, lizards), and opportunistic nectar-feeding behavior. Different life modes should promote a low functional equivalence among pollinators, while opportunistic nectar feeding would lead to reduced and unpredictable pollination effectiveness (PE) compared to more specialized nectarivores.

Dissecting the quantity (QNC) and quality (QLC) components of PE, we studied the opportunistic bird–lizard pollinator assemblage of Isoplexis canariensis from the Canary Islands to experimentally evaluate these potential characteristics. Birds and lizards showed different positions in the PE landscape, highlighting their low functional equivalence. Birds were more efficient than lizards due to higher visitation frequency (QNC). Adult lizards differed from juveniles in effecting a higher production of viable seeds (QLC). The disparate life modes of birds and lizards resulted in ample intra- and inter-specific PE variance. The main sources of PE variance were visitation frequency (both lizards and birds), number of flowers probed (lizards) and proportion of viable seeds resulting from a single visit (birds).

The non-coincident locations of birds and lizards on the PE landscape indicate potential constraints for effectiveness. Variations in pollinator abundance can result in major effectiveness shifts only if QLC is relatively high, while changes in QLC would increase PE substantially only at high QNC. The low functional equivalence of impoverished, highly contrasted pollinator assemblages may be an early diagnostic signal for pollinator extinction potentially driving the collapse of mutualistic services.

Muriquis

Muriquis (Brachyteles arachnoides) are the largest neotropical primates and the largest mammal endemic to Brazil, reaching more than 12 kg (Reis et al., 2006). They are endemic to the SE Brazil.

Previously recorded as different subspecies, muriquis are currently recognized as two distinct species, the northern muriqui B. hypoxanthus and southern muriqui B. arachnoides (Rylands et al., 1997). Aguirre (1971) estimated that before the arrival of Europeans there were about 400,000 muriquis in the Atlantic rainforest, distributed from southern Bahia to northern Paraná, and in 1971 there were no more than 3,000 individuals. Currently the northern muriqui occurs in southern Bahia, Espirito Santo and Minas Gerais and the southern muriqui occurs in southern Rio de Janeiro, São Paulo and northern Paraná (Melo and Dias 2005, Hirsch et al., 2006).

The muriquis live in groups of more than 30 individuals present social fission-fusion system where the group is divided into independent sub-groups of variable size. When in pristine areas they have a higher home ranges, ca. 1000ha, within daily displacements more than 5 km. I was fortunate enough to watch a group of 10-11 muriquis in Intervales, relatively close to the Carmo base. They were 3 males, 2-3 juveniles and 3 females, two of them carrying babies. Some of the individuals were feeding on the catkins of Cecropia glazeouvi. I approached them on a very steep slope and observed them for ca. 30 min. They were moving slowly among the canopies of the trees but with an extraordinary agility, always helping themselves with the tail. After a period close to me they moved quickly uphill.

Muriquis are herbivores, adapted to the handling, chewing and digestion of leaves or fleshy fruits, and they also consume flowers, seeds and bamboo (Strier 1991; Talebi et al., 2005). In relation to frugivory, muriquis have lower consumption of fruits (21% to 33%) in semi-deciduous Atalantic forest (Strier 1991, Martins 2006, 2008), but more intense consumption (35% to 71%) in ombrophilous Atlantic rain forests (Petroni 1993, 2000, Carvalho et al ., 2004; Talebi et al., 2005).

My friend Rafael Bueno did his master project (finished in 2010) on this species and tapirs [Frugivoria e efetividade de dispersão de sementes dos últimos grandes frugívoros da Mata Atlântica: a anta (Tapirus terrestris) e o muriqui (Brachyteles arachnoides)]. He did a great job showing the relevance of these frugivores for the dynamics of the Atlantic forest. Many tree species (at least 28 species) critically depend on their service for seed dispersal. Rafael recorded daily movements of muriqui groups ranging between 0.5 and 5.4 km. He estimated that on average, individual muriquis may disperse ca. 11,000 seeds/year. These amazing data show how relevant plant-animal mutualistic interactions are for the maintenance of tropical forests.