Insular dwarfism

Insular dwarfism, a form of phyletic dwarfism,[1] is the process and condition of large animals evolving or having a reduced body size[lower-alpha 1] 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"). 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.

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.

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. atacisIbero-Armorican IslandLate Cretaceous / Maastrichtian
Nemegtosaurids

Europasaurus		E. holgeriLower SaxonyLate Jurassic / Middle Kimmeridgian
Brachiosaurs

Magyarosaurus		M. dacusHateg IslandLate Cretaceous / Maastrichtian
Rapetosaurus

Lirainosaurus[11]		L. astibiaeIbero-Armorican IslandLate Cretaceous

Paludititan		P. nalatzensisHateg IslandLate Cretaceous / Maastrichtian
Epachthosaurus

Other
Example Species Range Time frame Continental relative

Langenberg Quarry
torvosaur (blue)		UnnamedLower SaxonyLate Jurassic / Middle Kimmeridgian
Torvosaurus

Struthiosaurus[12]		S. austriacus

S. transylvanicus

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

Telmatosaurus		T. transsylvanicusHateg IslandLate Cretaceous
Hadrosaurids

Thecodontosaurus[9]		T. antiquusSouthern EnglandLate Triassic / Rhaetian
Plateosaurs

Zalmoxes[9] (purple)		Z. robustus

Z. shqiperorum		Hateg IslandLate 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 glenosMolokaiExtinct (Late Quaternary)
American ibises
Apteribis brevisMaui
Cozumel curassow[13]Crax rubra griscomiCozumelUnknown
Great curassow

Kangaroo Island emu[14]		Dromaius novaehollandiae baudinianusKangaroo Island, South AustraliaExtinct (c. AD 1827)
Emu

King Island emu[15] (black)		Dromaius novaehollandiae minorKing Island, TasmaniaExtinct (AD 1822)LR ≈ 0.48 [lower-alpha 2]
Dwarf yellow eyed penguin[16]Megadyptes antipodes richdaleiChatham Islands, New ZealandExtinct (after 1300 AD)
Yellow-eyed penguin

Cozumel thrasher[13]		Toxostoma gluttatumCozumelCritically endangered
Other thrashers

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

Madagascar dwarf chameleon		Brookesia minimaNosy Be island, MadagascarEndangered
Madagascar leaf chameleons

Nosy Hara chameleon[17]		Brookesia micraNosy Hara island, MadagascarVulnerable
Roxby Island tiger snake[5]Notechis scutatusRoxby Island, South AustraliaUnknown
Tiger snake
Dwarf Burmese python Python bivittatus progschaiJava, Bali, Sumbawa and Sulawesi, IndonesiaUnknown
Burmese python		LR ≈ 0.44 [lower-alpha 3]
Tanahjampea reticulated python[20] Python reticulatus jampeanusTanahjampea, between Sulawesi and FloresUnknown
Reticulated python		LR ≈ 0.41, males
LR ≈ 0.49, females [lower-alpha 4]

Pilosans
Example Binomial name Native range Status Continental relative

Pygmy three-toed sloth		Bradypus pygmaeusIsla Escudo de Veraguas, PanamaCritically endangered
Brown-throated sloth

Acratocnus		A. antillensis

A. odontrigonus

A. ye		Cuba, Hispaniola and Puerto RicoExtinct (c. 3000 BC)
Continental ground sloths
ImagocnusI. zazaeCubaExtinct (Early Miocene)

Megalocnus		M. rodens

M. zile		Cuba and HispaniolaExtinct (c. 2700 BC)

Neocnus		Neocnus spp.Cuba and HispaniolaExtinct (c. 3000 BC)

Proboscideans
Main article: Dwarf elephant
Example Binomial name Native range Status Continental relative
Sulawesi dwarf elephantElephas celebensisSulawesiExtinct (Early Pleistocene)
Asian elephant

Cabarruyan dwarf elephant		Elephas beyeriLuzonExtinct

Cretan dwarf mammoth		Mammuthus creticusCreteExtinct
Mammuthus

Channel Islands mammoth		Mammuthus exilisSanta Rosae islandExtinct (Late Pleistocene)
Columbian mammoth
Sardinian mammothMammuthus lamarmoraiSardiniaExtinct (Late Pleistocene)
Steppe mammoth
Saint Paul Island woolly mammoth[23][24]Mammuthus primigeniusSaint Paul Island, AlaskaExtinct (c. 3750 BC)
Woolly mammoth

Siculo-Maltese elephants		Palaeoloxodon antiquus leonardi

P. mnaidriensis

P. melitensis

P. falconeri		Sicily and MaltaExtinct
Straight-tusked elephant
(left)
Cretan elephantsPalaeoloxodon chaniensis

P. creutzburgi		CreteExtinct

Cyprus dwarf elephant		Palaeoloxodon cypriotesCyprusExtinct (c. 9000 BC)
Naxos dwarf elephantPalaeoloxodon sp.NaxosExtinct
Rhodes and Tilos dwarf elephantPalaeoloxodon tiliensisRhodes and TilosExtinct
Bumiayu dwarf sinomastodont[25]Sinomastodon bumiajuensisBumiayu 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 florensisFloresExtinct (Late Pleistocene)
Sundaland Stegodon
Javan dwarf stegodontsStegodon hypsilophus[25]

S. semedoensis[29]

S. sp.[25]		JavaExtinct (Quaternary)
Mindanao pygmy stegodont[30]Stegodon mindanensisMindanao and SulawesiExtinct (Middle Pleistocene)
Sulawesi dwarf stegodont[25]Stegodon sompoensisSulawesiExtinct
Lesser Flores dwarf stegodont[3]Stegodon sondaariFloresExtinct (Middle Pleistocene)
Sumba dwarf stegodont[31]Stegodon sumbaensisSumba, IndonesiaExtinct (Middle Pleistocene)
Timor dwarf stegodont[25]Stegodon timorensisTimorExtinct
Dwarf stegolophodont[32]Stegolophodon pseudolatidensJapanExtinct (Miocene)
Stegolophodon

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

Flores Man[34]		Homo floresiensisFloresExtinct (Late Pleistocene)
Homo erectus

Callao Man		Homo luzonensis[35][36]Luzon, PhilippinesExtinct (Late Pleistocene)
Modern pygmies of Flores[37]Homo sapiensFloresExtantother members of Homo sapiens
Early Palau modern humans (disputed)[38]Homo sapiensPalauExtinct (?)
Andamanese[39]Homo sapiensAndaman IslandsExtant

Sardinian macaque[40]		Macaca majoriSardiniaExtinct (Pleistocene)
Barbary macaque

Zanzibar red colobus		Piliocolobus kirkiiUngujaEndangered
Udzungwa red colobus

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

Sicilian wolf		Canis lupus cristaldiiSicilyExtinct (AD 1970)
Gray wolf

Japanese wolf		Canis lupus hodophilaxJapan (excluding Hokkaido)Extinct (AD 1905)

Sardinian dhole
(forward)		Cynotherium sardousCorsica and SardiniaExtinct (c. 8300 BC)
Xenocyon
Trinil dogMececyon trinilensisJavaExtinct (Pleistocene)
Cozumel Island coati[13]Nasua narica nelsoniCozumelCritically endangered
Yucatan white-nosed coati

Zanzibar leopard		Panthera pardus pardusUngujaCritically endangered or Extinct
African leopard

Bali tiger		Panthera tigris sondaicaBaliExtinct (c. AD 1940)
Sumatran tiger

Javan tiger		JavaExtinct (c. AD 1975)

Cozumel raccoon		Procyon pygmaeusCozumelCritically endangered
Common raccoon

Island fox		Urocyon littoralisSix of the Channel Islands of CaliforniaNear Threatened
Gray fox		LR ≈ 0.84 [lower-alpha 5]
LR ≈ 0.75 [lower-alpha 6]
Cozumel foxUrocyon sp.CozumelCritically endangered or Extinct

Non-ruminant ungulates
Example Binomial name Native range Status Continental relative

Eumaiochoerus		Eumaiochoerus etruscusBaccinello, MontebamboliExtinct (Miocene)
Microstonyx

Malagasy dwarf hippopotamuses		Hippopotamus laloumena

H. lemerlei

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

Cretan dwarf hippopotamus		Hippopotamus creutzburgiCreteExtinct (Middle Pleistocene)
European hippopotamus

Maltese dwarf hippopotamus		Hippopotamus melitensisMaltaExtinct (Pleistocene)

Cyprus dwarf hippopotamus		Hippopotamus minorCyprusExtinct (c. 8000 BC)

Sicilian dwarf hippopotamus		Hippopotamus pentlandiSicilyExtinct (Pleistocene)
Cozumel collared peccary[13]Pecari tajacu nanusCozumelUnknown
Collared peccary
Philippine rhinoceros[43]Nesorhinus philippinensisLuzonExtinct (Middle Pleistocene)
Javan rhinoceros

Bovids
Example Binomial name Native range Status Continental relative
Sicilian bison[26]Bison priscus siciliaeSicilyExtinct (Late Pleistocene)
Steppe bison
Sicilian aurochs[44]Bos primigenius siciliae[26]SicilyExtinct (Late Pleistocene)
Eurasian aurochs
Cebu tamarawBubalus cebuensisCebu, PhilippinesExtinct
Wild water buffalo

Lowland anoa		Bubalus depressicornisSulawesi and Buton, IndonesiaEndangered
Bubalus grovesiBubalus grovesiSulawesi, IndonesiaExtinct

Tamaraw		Bubalus mindorensisMindoro, PhilippinesCritically endangered

Mountain anoa		Bubalus quarlesiSulawesi and Buton, IndonesiaEndangered

Balearic Islands cave goat		Myotragus balearicusMajorca and MenorcaExtinct (after 3000 BC)Gallogoral
Nesogoral[45]Nesogoral spp.SardiniaExtinct
Dahlak Kebir gazelle[46]Nanger soemmerringi ssp.Dahlak Kebir island, EritreaVulnerable
Soemmerring's gazelle

Tyrrhenotragus		Tyrrhenotragus gracillimusBaccinelloExtinctAntilopinae sp.

Cervids and relatives
Example Binomial name Native range Status Continental relative

Cretan dwarf megacerines[lower-alpha 7]		Candiacervus spp.CreteExtinct (Pleistocene)
Praemegaceros verticornis[9]

Sardinian megacerine[9]		Praemegaceros caziotiSardiniaExtinct (c. 5500 BC)

Ryukyu dwarf deer[49]		Cervus astylodonRyukyu IslandsExtinct
Sika deer (?)

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

Corsican red deer		Cervus elaphus corsicanusCorsica and SardiniaNear Threatened
Pleistocene Sicilian deer[26]Cervus siciliaeSicilyExtinct (Late Pleistocene)

Hoplitomeryx[lower-alpha 8]		Hoplitomeryx spp.Gargano IslandExtinct (Early Pliocene)
Pecorans
Sicilian megacerine[26]Megaloceros carburangelensisSicilyExtinct (Late Pleistocene)
Irish elk

Florida Key deer		Odocoileus virginianus claviumFlorida KeysEndangered
Virginia deer

Svalbard reindeer		Rangifer tarandus platyrhynchusSvalbardVulnerable
Reindeer

Philippine deer		Rusa mariannaPhilippinesVulnerable
Sambar deer

Plants
Possible example Binomial name Native range Status Continental relative

Insular elephant cacti[51][52]		Pachycereus pringleiRemote 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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