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Insular dwarfism

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For other uses, see Dwarf (disambiguation).
Skeletons of Malta's extinct Palaeoloxodon falconeri, the smallest known species of elephant. Adult males measured about one meter in shoulder height and weighed about 305 kg. Females were smaller.

Insular dwarfism, a form of phyletic dwarfism,[1] is the process and condition of large animals evolving or having a reduced body size[a] when their population's range is limited to a small environment, primarily islands. This natural process is distinct from the intentional creation of dwarf breeds, called dwarfing. This process has occurred many times throughout evolutionary history, with examples including dinosaurs, like Europasaurus and Magyarosaurus dacus, and modern animals such as elephants and their relatives. This process, and other "island genetics" artifacts, can occur not only on islands, but also in other situations where an ecosystem is isolated from external resources and breeding. This can include caves, desert oases, isolated valleys and isolated mountains ("sky islands").[citation needed] Insular dwarfism is one aspect of the more general "island effect" or "Foster's rule", which posits that when mainland animals colonize islands, small species tend to evolve larger bodies (island gigantism), and large species tend to evolve smaller bodies. This is itself one aspect of island syndrome, which describes the differences in morphology, ecology, physiology and behaviour of insular species compared to their continental counterparts.

Possible causes

There are several proposed explanations for the mechanism which produces such dwarfism.[3][4]

One is a selective process where only smaller animals trapped on the island survive, as food periodically declines to a borderline level. The smaller animals need fewer resources and smaller territories, and so are more likely to get past the break-point where population decline allows food sources to replenish enough for the survivors to flourish. Smaller size is also advantageous from a reproductive standpoint, as it entails shorter gestation periods and generation times.[3]

In the tropics, small size should make thermoregulation easier.[3]

Among herbivores, large size confers advantages in coping with both competitors and predators, so a reduction or absence of either would facilitate dwarfing; competition appears to be the more important factor.[4]

Among carnivores, the main factor is thought to be the size and availability of prey resources, and competition is believed to be less important.[4] In tiger snakes, insular dwarfism occurs on islands where available prey is restricted to smaller sizes than are normally taken by mainland snakes. Since prey size preference in snakes is generally proportional to body size, small snakes may be better adapted to take small prey.[5]

Dwarfism vs. gigantism

The inverse process, wherein small animals breeding on isolated islands lacking the predators of large land masses may become much larger than normal, is called island gigantism. An excellent example is the dodo, the ancestors of which were normal-sized pigeons. There are also several species of giant rats, one still extant, that coexisted with both Homo floresiensis and the dwarf stegodonts on Flores.

The process of insular dwarfing can occur relatively rapidly by evolutionary standards. This is in contrast to increases in maximum body size, which are much more gradual. When normalized to generation length, the maximum rate of body mass decrease during insular dwarfing was found to be over 30 times greater than the maximum rate of body mass increase for a ten-fold change in mammals.[6] The disparity is thought to reflect the fact that pedomorphism offers a relatively easy route to evolve smaller adult body size; on the other hand, the evolution of larger maximum body size is likely to be interrupted by the emergence of a series of constraints that must be overcome by evolutionary innovations before the process can continue.[6]

Factors influencing the extent of dwarfing

For both herbivores and carnivores, island size, the degree of island isolation and the size of the ancestral continental species appear not to be of major direct importance to the degree of dwarfing.[4] However, when considering only the body masses of recent top herbivores and carnivores, and including data from both continental and island land masses, the body masses of the largest species in a land mass were found to scale to the size of the land mass, with slopes of about 0.5 log(body mass/kg) per log(land area/km2).[7] There were separate regression lines for endothermic top predators, ectothermic top predators, endothermic top herbivores and (on the basis of limited data) ectothermic top herbivores, such that food intake was 7 to 24-fold higher for top herbivores than for top predators, and about the same for endotherms and ectotherms of the same trophic level (this leads to ectotherms being 5 to 16 times heavier than corresponding endotherms).[7]

Examples

Non-avian dinosaurs

Recognition that insular dwarfism could apply to dinosaurs arose through the work of Ferenc Nopcsa, a Hungarian-born aristocrat, adventurer, scholar, and paleontologist. Nopcsa studied Transylvanian dinosaurs intensively, noticing that they were smaller than their cousins elsewhere in the world. For example, he unearthed six-meter-long sauropods, a group of dinosaurs which elsewhere commonly grew to 30 meters or more. Nopcsa deduced that the area where the remains were found was an island, Hațeg Island (now the Haţeg or Hatzeg basin in Romania) during the Mesozoic era.[8][9] Nopcsa's proposal of dinosaur dwarfism on Hațeg Island is today widely accepted after further research confirmed that the remains found are not from juveniles.[10]

Sauropods

Example Species Range Time frame Continental relative

Ampelosaurus		 A. atacis Ibero-Armorican Island Late Cretaceous / Maastrichtian
Nemegtosaurids

Europasaurus		 E. holgeri Lower Saxony Late Jurassic / Middle Kimmeridgian
Brachiosaurs

Magyarosaurus		 M. dacus Hateg Island Late Cretaceous / Maastrichtian
Rapetosaurus

Lirainosaurus[11]		 L. astibiae Ibero-Armorican Island Late Cretaceous

Paludititan		 P. nalatzensis Hateg Island Late Cretaceous / Maastrichtian
Epachthosaurus

Other

Example Species Range Time frame Continental relative

Langenberg Quarry
torvosaur (blue)		 Unnamed Lower Saxony Late Jurassic / Middle Kimmeridgian
Torvosaurus

Struthiosaurus[12]		 S. austriacus

S. transylvanicus

S. languedocensis		 Ibero-Armorican, Australoalpine, and Hateg islands Late Cretaceous
Edmontonia

Telmatosaurus		 T. transsylvanicus Hateg Island Late Cretaceous
Hadrosaurids

Thecodontosaurus[9]		 T. antiquus Southern England Late Triassic / Rhaetian
Plateosaurs

Zalmoxes[9] (purple)		 Z. robustus

Z. shqiperorum		 Hateg Island Late Cretaceous
Tenontosaurus

In addition, the genus Balaur was initially described as a Velociraptor-sized dromaeosaurid (and in consequence a dubious example of insular dwarfism), but has been since reclassified as a secondarily flightless stem bird, closer to modern birds than Jeholornis (thus actually an example of insular gigantism).

Birds

Example Binomial name Native range Status Continental relative Insular / mainland
length or mass ratio

Hawaiian flightless ibises		 Apteribis glenos Molokai Extinct (Late Quaternary)
American ibises
Apteribis brevis Maui
Cozumel curassow[13] Crax rubra griscomi Cozumel Unknown
Great curassow

Kangaroo Island emu[14]		 Dromaius novaehollandiae baudinianus Kangaroo Island, South Australia Extinct (c. AD 1827)
Emu

King Island emu[15] (black)		 Dromaius novaehollandiae minor King Island, Tasmania Extinct (AD 1822) LR ≈ 0.48 [b]
Dwarf yellow eyed penguin[16] Megadyptes antipodes richdalei Chatham Islands, New Zealand Extinct (after 1300 AD)
Yellow-eyed penguin

Cozumel thrasher[13]		 Toxostoma gluttatum Cozumel Critically endangered
Other thrashers

Squamates

Example Binomial name Native range Status Continental relative Insular / mainland
length or mass ratio

Madagascar dwarf chameleon		 Brookesia minima Nosy Be island, Madagascar Endangered
Madagascar leaf chameleons

Nosy Hara chameleon[17]		 Brookesia micra Nosy Hara island, Madagascar Vulnerable
Roxby Island tiger snake[5] Notechis scutatus Roxby Island, South Australia Unknown
Tiger snake
Dwarf Burmese python Python bivittatus progschai Java, Bali, Sumbawa and Sulawesi, Indonesia Unknown
Burmese python		 LR ≈ 0.44 [c]
Tanahjampea reticulated python[20] Python reticulatus jampeanus Tanahjampea, between Sulawesi and Flores Unknown
Reticulated python		 LR ≈ 0.41, males
LR ≈ 0.49, females [d]

Mammals

Pilosans

Example Binomial name Native range Status Continental relative

Pygmy three-toed sloth		 Bradypus pygmaeus Isla Escudo de Veraguas, Panama Critically endangered
Brown-throated sloth

Acratocnus		 A. antillensis

A. odontrigonus

A. ye		 Cuba, Hispaniola and Puerto Rico Extinct (c. 3000 BC)
Continental ground sloths
Imagocnus I. zazae Cuba Extinct (Early Miocene)

Megalocnus		 M. rodens

M. zile		 Cuba and Hispaniola Extinct (c. 2700 BC)

Neocnus		 Neocnus spp. Cuba and Hispaniola Extinct (c. 3000 BC)

Proboscideans

Main article: Dwarf elephant
Example Binomial name Native range Status Continental relative
Sulawesi dwarf elephant Elephas celebensis Sulawesi Extinct (Early Pleistocene)
Asian elephant

Cabarruyan dwarf elephant		 Elephas beyeri Luzon Extinct

Cretan dwarf mammoth		 Mammuthus creticus Crete Extinct
Mammuthus

Channel Islands mammoth		 Mammuthus exilis Santa Rosae island Extinct (Late Pleistocene)
Columbian mammoth
Sardinian mammoth Mammuthus lamarmorai Sardinia Extinct (Late Pleistocene)
Steppe mammoth
Saint Paul Island woolly mammoth[23][24] Mammuthus primigenius Saint Paul Island, Alaska Extinct (c. 3750 BC)
Woolly mammoth

Siculo-Maltese elephants		 Palaeoloxodon antiquus leonardi

P. mnaidriensis

P. melitensis

P. falconeri		 Sicily and Malta Extinct
Straight-tusked elephant
(left)
Cretan elephants Palaeoloxodon chaniensis

P. creutzburgi		 Crete Extinct

Cyprus dwarf elephant		 Palaeoloxodon cypriotes Cyprus Extinct (c. 9000 BC)
Naxos dwarf elephant Palaeoloxodon sp. Naxos Extinct
Rhodes and Tilos dwarf elephant Palaeoloxodon tiliensis Rhodes and Tilos Extinct
Bumiayu dwarf sinomastodont[25] Sinomastodon bumiajuensis Bumiayu Island (now part of Java) Extinct (Early Pleistocene)
Sinomastodon

Japanese stegodont[26][27]		 Stegodon miensis

Stegodon protoaurorae

Stegodon aurorae		 Japan (Also Taiwan for S. aurorae)[28] Extinct (Early Pleistocene)
Chinese Stegodon
Greater Flores dwarf stegodont[3] Stegodon florensis Flores Extinct (Late Pleistocene)
Sundaland Stegodon
Javan dwarf stegodonts Stegodon hypsilophus[25]

S. semedoensis[29]

S. sp.[25]		 Java Extinct (Quaternary)
Mindanao pygmy stegodont[30] Stegodon mindanensis Mindanao and Sulawesi Extinct (Middle Pleistocene)
Sulawesi dwarf stegodont[25] Stegodon sompoensis Sulawesi Extinct
Lesser Flores dwarf stegodont[3] Stegodon sondaari Flores Extinct (Middle Pleistocene)
Sumba dwarf stegodont[31] Stegodon sumbaensis Sumba, Indonesia Extinct (Middle Pleistocene)
Timor dwarf stegodont[25] Stegodon timorensis Timor Extinct
Dwarf stegolophodont[32] Stegolophodon pseudolatidens Japan Extinct (Miocene)
Stegolophodon

Primates

Example Binomial name Native range Status Continental relative
Nosy Hara dwarf lemur[33] Cheirogaleus sp. Nosy Hara island off Madagascar Unknown
Dwarf lemurs

Flores Man[34]		 Homo floresiensis Flores Extinct (Late Pleistocene)
Homo erectus

Callao Man		 Homo luzonensis[35][36] Luzon, Philippines Extinct (Late Pleistocene)
Modern pygmies of Flores[37] Homo sapiens Flores Extant other members of Homo sapiens
Early Palau modern humans (disputed)[38] Homo sapiens Palau Extinct (?)
Andamanese[39] Homo sapiens Andaman Islands Extant

Sardinian macaque[40]		 Macaca majori Sardinia Extinct (Pleistocene)
Barbary macaque

Zanzibar red colobus		 Piliocolobus kirkii Unguja Endangered
Udzungwa red colobus

Carnivorans

Example Binomial name Native range Status Continental relative Insular / mainland
length or mass ratio

Sicilian wolf		 Canis lupus cristaldii Sicily Extinct (AD 1970)
Gray wolf

Japanese wolf		 Canis lupus hodophilax Japan (excluding Hokkaido) Extinct (AD 1905)

Sardinian dhole
(forward)		 Cynotherium sardous Corsica and Sardinia Extinct (c. 8300 BC)
Xenocyon
Trinil dog Mececyon trinilensis Java Extinct (Pleistocene)
Cozumel Island coati[13] Nasua narica nelsoni Cozumel Critically endangered
Yucatan white-nosed coati

Zanzibar leopard		 Panthera pardus pardus Unguja Critically endangered or Extinct
African leopard

Bali tiger		 Panthera tigris sondaica Bali Extinct (c. AD 1940)
Sumatran tiger

Javan tiger		 Java Extinct (c. AD 1975)

Cozumel raccoon		 Procyon pygmaeus Cozumel Critically endangered
Common raccoon

Island fox		 Urocyon littoralis Six of the Channel Islands of California Near Threatened
Gray fox		 LR ≈ 0.84 [e]
LR ≈ 0.75 [f]
Cozumel fox Urocyon sp. Cozumel Critically endangered or Extinct

Non-ruminant ungulates

Example Binomial name Native range Status Continental relative

Eumaiochoerus		 Eumaiochoerus etruscus Baccinello, Montebamboli Extinct (Miocene)
Microstonyx

Malagasy dwarf hippopotamuses		 Hippopotamus laloumena

H. lemerlei

H. madagascariensis		 Madagascar Extinct (c. AD 1000)
Common hippopotamus
Bumiayu dwarf hippopotamus[25] Hexaprotodon simplex Bumiayu Island (now Java) Extinct (Early Pleistocene)
Asian hippopotamuses

Cretan dwarf hippopotamus		 Hippopotamus creutzburgi Crete Extinct (Middle Pleistocene)
European hippopotamus

Maltese dwarf hippopotamus		 Hippopotamus melitensis Malta Extinct (Pleistocene)

Cyprus dwarf hippopotamus		 Hippopotamus minor Cyprus Extinct (c. 8000 BC)

Sicilian dwarf hippopotamus		 Hippopotamus pentlandi Sicily Extinct (Pleistocene)
Cozumel collared peccary[13] Pecari tajacu nanus Cozumel Unknown
Collared peccary
Philippine rhinoceros[43] Nesorhinus philippinensis Luzon Extinct (Middle Pleistocene)
Javan rhinoceros

Bovids

Example Binomial name Native range Status Continental relative
Sicilian bison[26] Bison priscus siciliae Sicily Extinct (Late Pleistocene)
Steppe bison
Sicilian aurochs[44] Bos primigenius siciliae[26] Sicily Extinct (Late Pleistocene)
Eurasian aurochs
Cebu tamaraw Bubalus cebuensis Cebu, Philippines Extinct
Wild water buffalo

Lowland anoa		 Bubalus depressicornis Sulawesi and Buton, Indonesia Endangered
Bubalus grovesi Bubalus grovesi Sulawesi, Indonesia Extinct

Tamaraw		 Bubalus mindorensis Mindoro, Philippines Critically endangered

Mountain anoa		 Bubalus quarlesi Sulawesi and Buton, Indonesia Endangered

Balearic Islands cave goat		 Myotragus balearicus Majorca and Menorca Extinct (after 3000 BC) Gallogoral
Nesogoral[45] Nesogoral spp. Sardinia Extinct
Dahlak Kebir gazelle[46] Nanger soemmerringi ssp. Dahlak Kebir island, Eritrea Vulnerable
Soemmerring's gazelle

Tyrrhenotragus		 Tyrrhenotragus gracillimus Baccinello Extinct Antilopinae sp.

Cervids and relatives

Example Binomial name Native range Status Continental relative

Cretan dwarf megacerines[g]		 Candiacervus spp. Crete Extinct (Pleistocene)
Praemegaceros verticornis[9]

Sardinian megacerine[9]		 Praemegaceros cazioti Sardinia Extinct (c. 5500 BC)

Ryukyu dwarf deer[49]		 Cervus astylodon Ryukyu Islands Extinct
Sika deer (?)

Cervus praenipponicus (?)
Jersey red deer population[50] Cervus elaphus jerseyensis Jersey Extinct (Pleistocene)
Red deer

Corsican red deer		 Cervus elaphus corsicanus Corsica and Sardinia Near Threatened
Pleistocene Sicilian deer[26] Cervus siciliae Sicily Extinct (Late Pleistocene)

Hoplitomeryx[h]		 Hoplitomeryx spp. Gargano Island Extinct (Early Pliocene)
Pecorans
Sicilian megacerine[26] Megaloceros carburangelensis Sicily Extinct (Late Pleistocene)
Irish elk

Florida Key deer		 Odocoileus virginianus clavium Florida Keys Endangered
Virginia deer

Svalbard reindeer		 Rangifer tarandus platyrhynchus Svalbard Vulnerable
Reindeer

Philippine deer		 Rusa marianna Philippines Vulnerable
Sambar deer

Plants

Possible example Binomial name Native range Status Continental relative

Insular elephant cacti[51][52]		 Pachycereus pringlei Remote islands in the Sea of Cortez
(e.g. Santa Cruz, San Pedro Mártir)		 Not evaluated
Mainland elephant cacti

See also

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Notes

  1. ^ An example of noninsular phyletic dwarfism is the evolution of the dwarfed marmosets and tamarins among New World monkeys, culminating in the appearance of the smallest example, Cebuella pygmaea.[2]
  2. ^ Based on the heights in Fig. 1 of Heupink et al., 2011[15]
  3. ^ Based on maximum lengths of 2.5 m for the dwarf form[18] and 5.74 m for the mainland form[19]
  4. ^ Based on maximum Tanahjampea python total lengths (TL) of 2.10 m for males and 3.35 m for females[20] and maximum southern Sumatra python snout to vent lengths (SVL) of 4.5 m for males and 6.1 m for females[21] with SVLs corrected to TLs by multiplying by a factor of 1.127, derived from the average relative tail length (0.113) of African and Indian rock pythons[22]
  5. ^ For nearby mainland gray foxes[41]
  6. ^ For mainland gray foxes in general[42]
  7. ^ Like Hoplitomeryx, Candiacervus appears to be an unusual case in that members of this genus evolved into insular species of a wide range of sizes, not only dwarf forms but also some that might be considered giants.[47][48]
  8. ^ Hoplitomeryx is evidently quite an unusual case, because members of this genus apparently evolved into both dwarf and giant insular forms on the same island(s).[47]

References

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  2. ^ Perelman, P.; et al. (2011). "A Molecular Phylogeny of Living Primates". PLOS Genetics. 7 (3): 1–17. doi:10.1371/journal.pgen.1001342. PMC 3060065. PMID 21436896.
  3. ^ a b c d e Van Den Bergh, Gerrit Dirk; Awe, Rokhus Due; Morwood, Michael John; Sutikna, Thomas; Jatmiko; Wahyu Saptomo, E. (May 2008). "The youngest Stegodon remains in Southeast Asia from the Late Pleistocene archaeological site Liang Bua, Flores, Indonesia". Quaternary International. 182 (1): 16–48. Bibcode:2008QuInt.182...16V. doi:10.1016/j.quaint.2007.02.001.
  4. ^ a b c d Raia, Pasquale; Meiri, Shai (August 2006). "The island rule in large mammals: paleontology meets ecology". Evolution. 60 (8): 1731–1742. doi:10.1111/j.0014-3820.2006.tb00516.x. PMID 17017072. S2CID 26853128.
  5. ^ a b Keogh, J. S.; Scott, I. A. W.; Hayes, C. (January 2005). "Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes". Evolution. 59 (1): 226–233. doi:10.1111/j.0014-3820.2005.tb00909.x. PMID 15792242. S2CID 58524.
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  16. ^ Cole, Theresa L., et al. "Mitogenomes uncover extinct penguin taxa and reveal island formation as a key driver of speciation." Molecular biology and evolution 36.4 (2019): 784-797.
  17. ^ Glaw, F.; Köhler, J.; Townsend, T. M.; Vences, M. (2012-02-14). "Rivaling the World's Smallest Reptiles: Discovery of Miniaturized and Microendemic New Species of Leaf Chameleons (Brookesia) from Northern Madagascar". PLoS ONE. 7 (2): e31314. Bibcode:2012PLoSO...731314G. doi:10.1371/journal.pone.0031314. PMC 3279364. PMID 22348069.
  18. ^ de Lang R, Vogel G (2005). The Snakes of Sulawesi: A Field Guide to the Land Snakes of Sulawesi with Identification Keys. Frankfurt Contributions to Natural History Band 25, Edition Chimaira 2005. ISBN 3-930612-85-2. pp. 23–27, 198–201.
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  23. ^ Schirber, Michael. Surviving Extinction: Where Woolly Mammoths Endured. Live Science. Imaginova Corporation. Retrieved 2007-07-20.
  24. ^ The mammoths of Wrangel Island, north of Siberia, are no longer considered dwarfs. See: Tikhonov, Alexei; Larry Agenbroad; Sergey Vartanyan (2003). Comparative analysis of the mammoth populations on Wrangel Island and the Channel Islands. DEINSEA 9: 415–420. ISSN 0923-9308
  25. ^ a b c d e f Aziz, F.; van den Bergh, G. D. (September 25, 1995). "A dwarf Stegodon from Sambungmacan (Central Java, Indonesia)". Proc. Kon. Ned. Akad. V. Wetensch. 98 (3): 229–241. Retrieved 2017-07-31.
  26. ^ a b c d e Sondaar, P. Y.; A.A.E. van der Geer (2005). "Evolution and Extinction of Plio-Pleistocene Island Ungulates". International Journal of the French Quaternary Association. 2: 241–256. Retrieved 2017-07-31.
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