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.

Extant Megafauna Frugivores

The end-Pleistocene mega-mammal extinction (also including other vertebrate groups) likely had a severe effect on present-day megafauna assemblages and impaired important functions associated with ecological interactions involving megafauna taxa. The extant mega-mammal faunas around the world are impoverished versions of the Pleistocene biota on most continents except- perhaps- Africa. In addition, mega-mammals are particularly hard hit by ongoing human-driven disturbances like deforestation, hunting, pollution, and animal trade.

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Extinct species (black) and extant species (green) of mammal megafauna in different continents, illustrating the main higher taxa. Stuart, A.J. (2014) Late Quaternary megafaunal extinctions on the continents: a short review. Geological Journal, 50, 338–363.

Extant frugivorous mega-mammals are represented in a few orders and families: Carnivora, Artiodactyla, Perissodactyla, Marsupalia, Proboscidea, and Primates. Yet they span a high diversity of body sizes, digestive systems, movement patterns, and foraging modes, presumably defining a wide range of ecological functions for plant dispersal.
The representation of extant mega-birds is much more restricted- strictly speaking, to the large Ratites (emus, cassowaries, ostrich) most of them consuming fruits to variable extents.

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Then, herps and fish have also a reduced representation, with large iguanas, varanid lizards and giant turtles, on one hand, and a few genera of very large frugivorous fishes.
The population densities, distribution areas, and even body sizes of these extant megafauna species are being severely reduced by both direct and indirect human influences. This is what we call the anthropocene, and the defaunation events associated to global change drivers such as deforestation. We are just starting to grasp the delayed consequences of this dramatic loss of biodiversity for the persistence of forests worldwide.

Illustration: Pedro Jordano, based on Stuart (2014). Photos: Kulpat Saralamba, Alicia Solana, Néstor Pérez-Méndez, Dennis Hansen.

Megafauna-Dependent Plants

How did megafauna-dependent plants survive after the demise of the giant Pleistocene seed dispersers? Before hand, be warned that coextinctions are very difficult to assess and demonstrate in nature, especially for certain groups (e.g., hosts and ectoparasites). Moreover, think of the myriad possibilities for plants to stay on place even with collapsed dispersal: just haphazard seed dispersal may help; or suboptimal fruit removal and sporadic dispersal by other, less reliable frugivores; or the dispersal being taken over by efficient frugivores (e.g., scatter-hoarders) yet with limitations in some aspect of the dispersal service (e.g., loss of long-distance dispersal events); or dispersal taken over by megafauna surrogates such as livestock; or just by relying on vegetative propagation; or maybe by just being used by humans… All these situations show up eventually when one examines the natural history details of present-day “megafauna-dependent” plants. Thus, at some point it is not surprising that documented coextinctions of plants following the loss of seed dispersers are so rare, if there is any.

Seeds of fruits from megafauna-dependent plants
Seeds of fruits from megafauna-dependent plants (the label, for scale, is ca. 11 cm long). From top left to bottom right: Pouteria ucucui (Sapotaceae), Attalea (Orbygnia) phalerata (Arecaceae), Scheelea martiana (Arecaceae), Theobroma grandiflora (Malvaceae) (two images), Pouteria pariry (Sapotaceae), Licania macrophyla (Chrysobalanaceae), Parinari montana (Chrysobalanaceae), Lacunaria jemmani (Quiinaceae), Pouteria macrocarpa (Sapotaceae), Phytelephas macrocarpa (Arecaceae), Caryocar villosum (Caryocaraceae), Theobroma sp. (Malvaceae), Raphia vinifera (Arecaceae), Lecythidaceae, and Theobroma speciosa (Malvaceae). Pedro Jordano; Museum Goeldi Herbarium, Belém, Pará, Brazil.

However, even if seed dispersal has not fully collapsed, and even if coextinctions have not been extensive, the consequences have been non-trivial for the plant species that lost their megafauna frugivores: increased clumping, increased population isolation, severily-limited gene flow via seed, loss of genetic diversity, markedly reduced effective population sizes (i.e., the number of adults effectively contributing progeny), and demographic bottlenecks. Much research is still needed to fully understand which are these “cryptic” consequences of collapsed seed dispersal mutualisms, yet there are good evidences that the demographic and population genetic consequences are non-trivial.

Collevatti, R., Grattapaglia, D. & Hay, J. (2003) Evidences for multiple maternal lineages of Caryocar brasiliense populations in the Brazilian Cerrado based on the analysis of chloroplast DNA sequences and microsatellite haplotype variation. Molecular Ecology, 12, 105–115.

Malhi, Y., Doughty, C.E., Galetti, M., Smith, F.A., Svenning, J.-C. & Terborgh, J.W. (2016) Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proceedings of the National Academy of Sciences USA, 113, 838–846.

McConkey, K.R., Brockelman, W.Y., Saralamba, C. & Nathalang, A. (2015) Effectiveness of primate seed dispersers for an “oversized” fruit, Garcinia benthamii. Ecology, 96, 2737–2747.

Hall, J.A. & Walter, G.H. (2014) Relative seed and fruit toxicity of the Australian cycads Macrozamia miquelii and Cycas ophiolitica: further evidence for a megafaunal seed dispersal syndrome in cycads, and its possible antiquity. Journal of Chemical Ecology, 40, 860–868.

Hall, J.A. & Walter, G.H. (2013) Seed dispersal of the Australian cycad Macrozamia miquelii (Zamiaceae): Are cycads megafauna-dispersed “grove forming” plants? American Journal of Botany, 100, 1127–1136.

Janzen, D.H. (1981) Enterolobium cyclocarpum seed passage rate and survival in horses, Costa Rican Pleistocene seed dispersal agents. Ecology, 62, 593–601.

Text and photos: Pedro Jordano. Seedlings and dung photos: Alicia Solana. Seed photos from Museum Goeldi Herbarium, Belém, Pará, Brazil.

Seed Dispersal Anachronisms

The pequi, Caryocar brasilense, is an example of a seed dispersal anachronism. The fruits (pequi, "skin with spines" in tupi-guarani), up to 10-12 cm in diameter, have internal spines in the pulp, surrounding the seeds. Each fruit has a single or very few large seeds resulting a large fruit with a hard pericarp. Field studies of fruit removal rates have reported extremely low actual dispersal of seeds away from maternal trees, the fruits simply rotting on the ground beneath the tree canopy. Virtually no diaspores are found buried by hoarding rodents, or preyed upon by these animals. Pequi is common in central Brazilian cerrado vegetation from southern Pará to Paraná and northern Paraguay. Photos by Mauricio Mercadante CC
The pequi, Caryocar brasilense, is an example of a seed dispersal anachronism. The fruits (pequi, “skin with spines” in tupi-guarani), up to 10-12 cm in diameter, have internal spines in the pulp, surrounding the seeds. Each fruit has a single or very few large seeds resulting a large fruit with a hard pericarp. Field studies of fruit removal rates have reported extremely low actual dispersal of seeds away from maternal trees, the fruits simply rotting on the ground beneath the tree canopy. Virtually no diaspores are found buried by hoarding rodents, or preyed upon by these animals. Pequi is common in central Brazilian cerrado vegetation from southern Pará to Paraná and northern Paraguay. Photos by Mauricio Mercadante CC

In 1982, Daniel H. Janzen and Paul S. Martin advanced the hypothesis that a number of plant species we see in present-day forests shows fruits and seed dispersal adaptations not consistent with their interactions with extant frugivores. Thus, only when we consider the extensive frugviory shown by the extinct Pleistocene megafauna (horses, toxodons, gomphoteres, mastodons, macrauchenias, etc.) we can understand how these species evolved the fruit traits we see nowadays. How then, did these tree and shrub species persist in the absence of the animal mutualists they required for population persistence? The core of the hypothesis expects these anachronic dispersal systems to be best explained by interactions with extinct animals, showing impaired dispersal resulting in altered seed dispersal dynamics.
Janzen and Martin defined seed dispersal anachronisms as those dispersal syndromes with fruit traits and phenological patterns best explained by interactions with extinct animals and offered some striking examples of Neotropical fruits with anachronic traits. These ‘‘unfit’’ species share fruit traits and phenological patterns that are at least in part not expected from their interactions with the extant frugivore community, but logically explained if we consider the extinction or local absence of the main frugivores.
Key traits of megafaunal fruits include 1) overbuilt design, with large seeds protected mechanically by thick and hard endocarp and indehiscence, with nutrient-rich pulp and external similarity to fruits eaten by extant large African/Asian mammals; 2) phenological segregation of ripening times throughout the year; 3) fruits falling to the ground upon ripening; 4) fruits unattractive or not very attractive to arboreal or flying frugivores; 5) a large proportion of the fruit crop rots on the tree without being consumed; 6) frugivores include a large coterie of seed predators that might act sporadically as legitimate dispersers; 7) fallen fruits are avidly eaten by introduced horses, pigs, and cattle; and 8) natural habitats of the plant species today are alluvial bottoms on gentle slopes, usually along forest edges with grassland.
It is clear that functional dispersal for many of these species operates in present-day neotropical communities by means of diplochorous and alternative seed dispersal systems involving other agents such as scatter-hoarding rodents, tapirs, cattle, some primates and even bats, as well as haphazard (runoff) and human-mediated dispersal. However, the loss of seed dispersal by extremely large mammals may imply marked shifts in the patterns and consequences of seed dispersal for these plant species. Ongoing and future research should unveil the signals of the “ghosts of past mutualisms”.

Guimarães Jr., P.R., Galetti, M. & Jordano, P. (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE, 3, e1745.
Janzen, D. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science, 215, 19–27.
Martin, P.S. & Klein, R.G. (1984) Quaternary Extinctions: a Prehistoric Revolution. University of Arizona Press, Tucson, AZ.

How To Make A Megafauna Fruit

Just make it big, very big. Well, it’s not just that…- yet we’ll probably agree that megafauna fruits are, in some sense, overbuilt.
If we take the two major types of fruits that extant megafauna consume (e.g., elephants, rhino, etc.), we find two distinct typoplogies. Both are extremely large-sized fruits forms. The first one is like a drupaceous mega-cherry, a large fruit with a single, or very few (i.e., up to three or four) large individual seeds; the second type is kind of a mega-tomato, a large fruit with many, really many (up to hundreds), tiny seeds. Fruits of the first type are usually 4-10 cm diameter; those of the second type are usually > 10 cm in diameter.

megafauna_functional-001
The two main typologies of (fleshy) fruits eaten by extant megafauna. We should add also the role megafauna had in dispersing seeds of herbs and grasses, as well as epizoochoric seeds like those of devil’s claw (genera Proboscidea, Martynia, and Ibicella, Martyniaceae). Illustration: Pedro Jordano. Photo: Kulpat Saralamba CC 3.0.

Why do these fruit types differ when compared to other ‘normal’ fuits? It is not simply that they are much larger. Their key characteristic is that, for a given number of seeds per fruit, they pack up seed sizes up to three orders of magnitude larger than ‘normal’ fruits. Thus, megafaunal fruits allowed plants to circumvent the trade-off between seed size and dispersal by relying on frugivores able to disperse enormous seed loads over long-distances.

Some fleshy fruited, megafaunal-dependent species illustrating size, shape, and color variation. a, Attalea speciosa, Arecaceae; b, Mouriri elliptica, Melastomataceae; c, Hymenaea stigonocarpa, Fabaceae; d, Genipa americana, Rubiaceae; e, Salacia elliptica, Celastraceae; f, Annona dioica, Annonaceae. Black reference line is 2 cm length. Photos: Pedro Jordano, Mauro Galetti and Camila Donatti (fruits).
Some fleshy fruited, megafaunal-dependent species from Brazil (Pantanal) illustrating size, shape, and color variation. a, Attalea speciosa, Arecaceae; b, Mouriri elliptica, Melastomataceae; c, Hymenaea stigonocarpa, Fabaceae; d, Genipa americana, Rubiaceae; e, Salacia elliptica, Celastraceae; f, Annona dioica, Annonaceae. Black reference line is 2 cm length. Photos: Pedro Jordano, Mauro Galetti and Camila Donatti.

In addition to these two types of megafaunal (fleshy) fruits, the extinct Pleistocene megafauna most likely also dispersed grass seeds and seeds attached to their fur (epizoochoric).

Barlow, C. (2001) Anachronistic fruits and the ghosts who haunt them. Arnoldia, 61, 14–21.
Bretting, P.K. 1986. Changes in fruit shape in Proboscidea parviflora ssp. parviflora (Martyniaceae) with domestication. Economic Botany, 40, 170-176.
Feer, F. (1995) Morphology of fruits dispersed by African forest elephants. 
African Journal of Ecology, 33, 279–284.
Guimarães Jr., P.R., Galetti, M. & Jordano, P. (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE, 3, e1745.
Janzen, D. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science, 215, 19–27.
Janzen, D. (1984) Dispersal of small seeds by big herbivores: foliage is the fruit. American Naturalist, 123, 338–353.

Extinct Megafauna Frugivores

The diversity of extinct megafauna frugivores was extremely high in different continents, and a number of them played a central role in the evolution of fruit traits we see today. While the largest South American extant mammal is the tapir (Baird’s, up to 400 kg), consider that 100% of megamammal species (body mass >1000 kg) and about 80% of large mammal species (those over 44 kg) from the Pleistocene South American fauna was extinct ca. 10-12 Kyr BP. At least 37 genera of mammals were eliminated, including most of the megafauna species (i.e., gomphotheres, camelids, ground sloths, glyptodonts, and toxodontids). All megamammals (37 species) and most large mammals (46 species) present during the late Lujanian (latest Pleistocene- earliest Holocene) became extinct in South America (around 30 genera of mammals vanished in North America, 17 in Australia, and 24 in Asia). In contrast, Africa lost 8 of 50 megamammal genera. Africa and Southern Asia are the only continental areas that have terrestrial mammals weighing over 1000 kg today.

A number of the extinct Pleistocene megamammals were herbivores, grazers, browsers, and certainly did include fruits in their diet, probably in large amounts, thus potentially acting as seed dispersers for a variety of plants. This fact has been evidenced from coprolites and isotopic analysis of fossil remains, with additional insight from comparative anatomy and morphology. Present-day plant-frugivore interactions still have the signals of these ghosts of evolution.

Haynes, G. (ed.). 2009. American megafaunal extinctions at the end of the Pleistocene. Springer, Berlin.

Barlow, C. 2000. The ghosts of evolution: nonsensical fruit, missing partners, and other ecological anachronisms. Basic Books, New York.

Illustration: Sinammonite @deviantart.com

Most of the species shown in this great illustration from Sinammonite (http://sinammonite.deviantart.com/) were frugivorous (probably with the exception of the large carnivores) and legitimate seed dispersers of their food plants. The figure is high-res; you may wnat to zoom-in and seek the species names by the numbers.

prehistoric_behemoth_by_sinammonite-d64jjn6

Prehistoric megafauna.
1. Chilotherium anderssoni: 1.4m
2. Ancylotherium sp.: 1.8m
3. Sinotherium lagrelii: 2.6m
4. Pachycrocuta brevirostris: 1m
5. Panthera tigris: 0.97m
6. Homotherium crenatidens: 1.1m
7. Xenosmilus hodsonaei: 1.1m
8. “Amerhippusscotti: 1.5m
9. Hipparion insperatum: 1.9m
10. Loxodonta atlantica: 3.5m
11. Stegodon zdanskyi: 3.9m
12. Ningxiatherium euryrhinu: 2.2m
13. Gigantopithecus blacki: 1.8m
14. Dinocrocuta gigantea: 1.4m
15. Amphimachairodus palander: 1.1m
16. Smilodon populator: 1.2m
17. Panthera atrox: 1.3m
18. Equus sussenbornensis: 1.8m
19. Elephas maximus: 2.9m
20. Dzungariotherium orgosense: 4.5m
21. Palaeoloxodon antiquus: 4m
22. Bison priscus: 2.1m
23. Equus capensis: 1.46m
24. Elasmotherium chaprovicum 2.8m
25. Mammuthus trogontherii: 4.5m
26. Proboscidipparion sinense: 1.8m
27. Plesippus enormis 1.65m
28. Ceratotherium cottoni: 1.8m
29. Diprotodon optatum: 1.9m
30. Palaeoloxodon recki: 4.5m
31. Mammut borsoni: 3.5m
32. Equus koobiforensis: 1.6m
33. Palorchestes azael: 1.3m
34. Sivapanthera pleistocaenica: 1m
35. Equus mosbachensis: 1.65m
36. Stephanorhinus kirchbergensis: 2m
37. Palaeotherium giganteum: 1.5m
38. Zygomaturus trilobus: 1.5m
39. Deinotherium giganteum: 3.5m
40. Paraceratherium lepidum: 4.5m
41. Mammuthus columbi: 4m
42. “Equusmajor: 1.78m
43. Coelodonta antiquitatis: 1.8m
44. Bubalus youngi: 1.8m
45. Dzungariotherium? tienshanense: 5m
46. Stegodon ganesa: 4m
47. Sinohippus robustus 1.3m
48. Panthera spelaea: 1.2m
49. Embolotherium andrewsi: 2.8m
50. Allohippus sanmeniensis: 1.8m
51. Elasmotherium caucasicum: 3m
52. “Equusgiganteus: 2.25m
53. Syncerus antiquus: 1.65m

 

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.

fig-9-cada-um

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”.