SCIENCE CHINA Life Sciences. A generalized model of island biogeography

Transcription

1 SCIENCE CHINA Life Sciences RESEARCH PAPERS November 2 Vol54 No: 55 6 doi: 7/s y A generalized model of island biogeography CHEN XiaoYong *, JIAO Jing & TONG Xin Deparmen of Environmenal Sciences, Tianong Naional Observaion Saion for Fores Ecosysems, Eas China Normal Universiy, Shanghai 262, China Received June 8, 2; acceped Sepember 3, 2 MacArhur and Wilson s equilibrium heory is one of he mos influenial heories in ecology Alhough evoluion on islands is o be imporan o island biodiversiy, speciaion has no been well inegraed ino island biogeography models By incorporaing speciaion and facors influencing i ino he MacArhur-Wilson model, we propose a generalized model unifying ecological and evoluionary processes and island feaures Inra-island speciaion may play an imporan role in boh island species richness and endemism, and he conribuion of speciaion o local species diversiy may evenually be greaer han ha of immigraion under cerain condiions Those condiions are relaed o he per species speciaion rae, per species exincion rae, and island feaures, and hey are independen of immigraion rae The model predics ha large islands will have a high, hough no he highes, proporional endemism when oher parameers are fixed Based on he generalized model, changes in species richness and endemism on an oceanic island over ime were prediced o be similar o empirical observaions Our model provides an ideal saring poin for re-evaluaing he role of speciaion and re-analyzing available daa on island species diversiy, especially hose biased by he MacArhur-Wilson model island biogeography, speciaion, immigraion, exincion, area, isolaion, species richness, island developmen Ciaion: Chen X Y, Jiao J, Tong X A generalized model of island biogeography Sci China Life Sci, 2, 54: 55 6, doi: 7/s y *Corresponding auhor ( xychen@desecnueducn) MacArhur and Wilson s equilibrium heory [,2] is one of he mos influenial heories in biogeography, ecology and conservaion biology [3,4] As he paradigm of island biogeography, his dynamic equilibrium heory explains emergen paerns of species richness and endemism on an island based on wo biogeographical processes (immigraion and exincion) and on wo physical feaures of he island (area and isolaion) [,2] This heory has srongly influenced oher fields of ecology and conservaion biology for fory years and has simulaed many hundreds of sudies on paerns of species richness in a grea variey of ecosysems and bioas [5] Evoluion on islands is hough o be imporan on he evoluionary ime scale [,2], bu i has no been well considered in he dynamic equilibrium model, even hough evoluion is commonly used o explain exraordinarily high numbers of endemic species [6,7] The role of speciaion in he species diversiy of oceanic islands has long been noed and frequenly emphasized [6,8 3] There have numerous aemps o link evoluionary and ecological dynamics building on he MacArhur-Wilson model [4,5] However, he challenge of combining evoluion, immigraion, exincion and island feaures has no been well fulfilled, and here have been repeaed calls for heoreicians o develop new models/heories [3,5,2,6] Using a simple model of island biogeography heory, we previously prediced he relaive conribuions of speciaion and immigraion o island species diversiy over ime [7] We also provided a heoreical explanaion for he posiive relaionship beween percenage endemism and species diversiy on islands In his paper, we exend he simple model o a more generalized one ha includes he impacs of boh biogeographical processes and island feaures The Auhor(s) 2 This aricle is published wih open access a Springerlinkcom lifescichinacom wwwspringercom/scp

2 56 Chen X Y, e al Sci China Life Sci November (2) Vol54 No Maerials and mehods As poined ou by MacArhur and Wilson [], species richness on an island is ulimaely deermined by hree biogeographical processes: immigraion, which adds species o he island from he mainland or oher islands; local speciaion, which leads o divergence wihin some species; and exincion, which eliminaes species from he island Island feaures, such as area and isolaion, may have an impac on hese processes Alhough many islands occur in archipelagos, o simplify he model, we rea an archipelago as an island, because migraion among islands of an archipelago occurs a much higher raes han ha beween he archipelago and he mainland or oher islands/archipelagos Wihou loss of generaliy, he numbers of new species added by immigraion (I ) and species eliminaed by exincion (E ) a ime can be expressed as [8,9] I I D A ( S S ), M I( ) E EDA S, I( ) where S M is he species richness on he mainland; S I() is he species richness on he island a ime ; I and E are per species immigraion and exincion raes, or immigraion and exincion coefficiens, respecively [2]; D and A are disance o he mainland and island area, respecively; and are posiive consans scaling he impacs of disance on immigraion and exincion, respecively; and and are posiive consans scaling he impacs of area on immigraion and exincion, respecively The impac of island area on immigraion, ie, he arge effec, and he impac of isolaion/disance on exincion, ie, he rescue effec [2], are also considered in he wo equaions When all oher parameers are fixed, larger islands have higher immigraion raes, and nearer islands have lower exincion raes To incorporae he impac of evoluion, we inroduce he conribuion of inra-island speciaion ino he model Speciaion adds new species and herefore increases species richness on he island Larger islands generally have higher speciaion raes [6,22 24], while isolaion decreases gene flow among islands or beween he island and he mainland, leading o increased differeniaion and more speciaion [24,25] Thus, we ake he following form o express he number of new species on an island added by speciaion ( ) a ime :, D A SI( ) where is he per species speciaion rae, or speciaion coefficien, ie, he number of species added by speciaion per uni ime per species To simplify he model, is assumed consan and are posiive consans scaling he impacs of area and isolaion on speciaion, respecively The smaller he value of or, he sligher he impac of island area or isolaion on speciaion Species diversiy on he island a ime + is (see []) SI( ) SI( ) IE Similar o our previous sudy [7], given SI (), we have he following equaion: S I() ID AS [ ( ID A EDA DA) ] M ID A EDA DA Given he very small values of I, E and, as well as small values of he facors scaling he impacs of isolaion and area, I D A E D A D A is much smaller han Therefore, when, he number of species added by immigraion and speciaion equals ha eliminaed by exincion, and we ge equilibrium richness on he island, ie, ID AS SI I D A E D A D A M Because our aim is o undersand he effec of speciaion on he species richness of islands, o simplify he model, we only consider speciaion on islands and ignore speciaion on he mainland To mee he generaliy of lower richness on islands han on he mainland, his means ha ED DA Neverheless, our model has capured he main properies of he island biogeography equilibrium model [2,8] For example, local species richness increases wih increasing island area (Figure ) and wih decreasing isolaion Obviously, inra-island speciaion increases island species diversiy (Figure ) Considering he impac of island area on speciaion, here will be a posiive relaionship beween Figure Effecs of speciaion, disance and area on island species richness 3 3 when SM, I 8, E 5, =5, =, =, and == Disances o he mainland are 25 (black lines) and 625 (red lines), respecively Solid and dashed lines show he resuls when speciaion is presen ( 3 2 and 5 ) and absen, respecively Species richness of he island increases wih island area and decreases wih disance o he mainland Speciaion increases richness on he island () (2)

3 Chen X Y, e al Sci China Life Sci November (2) Vol54 No 57 species richness and and beween species richness and island area, which has been frequenly observed in island sysems [26] 2 Resuls and discussion 2 Relaive conribuion of speciaion and immigraion o richness over ime Boh ecological and evoluionary processes conribue o he species richness of an island Generally, ecological processes are hough o be more imporan over he shor-erm, ecological ime scale, while evoluionary processes are criical over he long-erm, evoluionary ime scale More specifically, immigraion plays an imporan role in he increase in species diversiy in he early sages of an island, while speciaion is criical in increasing species richness a laer sages Because he number of new species added by immigraion decreases wih increasing species diversiy on he island, while he number added by speciaion increases [3], can we expec ha speciaion will evenually add more species han immigraion, and if so, when and under wha condiions will his happen? If we se speciaion o add more new species per uni ime han does immigraion, ie, I, hen DAS I( ) ID A( S S ) Therefore, we can easily obain he M I( ) DA EDA ID A DA ln( ID A EDA DA) ime: ln[(2 ) / ( )] This relaionship indicaes ha he criical ime a which speciaion adds more new species per uni ime han does immigraion is delayed by increasing exincion and occurs earlier wih increasing immigraion and speciaion This shif in relaive imporance of immigraion and speciaion o local diversiy over ime coincides wih empirical observaions In he early sages, colonizaion plays a much more imporan role in species accumulaion on newly-creaed or serilized islands [27] As ime passes, he number of new species added by migraion o he island decreases because he difference in species richness beween he island and mainland decreases However, he shif described above is condiional In addiion o he condiion above, he criical ime should mee 2DA EDA, or, 2 A D E which is independen of he immigraion coefficien (Figure 2) When hese condiions are me, he conribuion of speciaion o local species richness will evenually be larger han ha of immigraion When all oher parameers are fixed, he larger he island area, he smaller he per species speciaion rae needed o effec he shif For example, when 25, A 625, D=25 and, and even if he per species speciaion rae is as lile as % of he per Figure 2 Number of species per uni ime added by immigraion (solid lines) and speciaion (dashed lines), a =2 3 (black lines), (red lines), and 5 5 (blue lines), respecively, given S M =, I =8 3, E =5 3, D=25, q=5, ==5, ===, and A= When, 2 A D E speciaion evenually adds more new species per uni ime han immigraion does (black lines) When, 2 A D E he number of species added by speciaion equals ha by immigraion (red lines) A, 2 A D E speciaion always adds fewer new species han immigraion does (blue lines) species exincion rae, speciaion will evenually add more species han immigraion per uni ime This indicaes ha, even a low raes, local speciaion may play a crucial role in island species diversiy, especially on large islands, and herefore speciaion is much more imporan o island biodiversiy han previously hough [5] Alhough he occurrence of he shif is independen of he immigraion coefficien, i is relaed o disance, because isolaion impacs boh speciaion and exincion raes When >, ie, he increase in speciaion rae is larger han ha of he exincion rae, as isolaion increases, speciaion will add more species han immigraion on islands wih a disance of E D from he mainland MacArhur & Wilson [2] suggesed ha, near he ouer limi of he dispersal 2 A range of a given axon where i has a low immigraion rae, he speciaion rae can exceed he immigraion rae Their saemen was correc, no because remoe islands have very low immigraion raes, bu because he disance affecs boh speciaion and exincion raes However, if < on an island wih a disance o he mainland smaller han 2 A E, speciaion may also add more species han

4 58 Chen X Y, e al Sci China Life Sci November (2) Vol54 No immigraion does afer a cerain ime This means ha, when he impac of disance on he exincion rae is sronger han on he speciaion rae, a disan island has oo much exincion o accumulae species diversiy, and he difference in species richness beween he island and he mainland is very large, leading o high immigraion pressure from he mainland Thus, he conribuion of immigraion o local species richness is larger han ha of speciaion However, on a near island, a high rae of immigraion o he island decreases he difference in richness beween he mainland and he island, and hus here are few immigrans per uni ime afer a cerain ime, while he speciaion rae coninues o rise as species numbers increase Therefore, he conribuion of speciaion o local richness on he island is larger han ha of immigraion 22 Island endemism The presence of abundan endemic species is one of he mos emergen properies of island biodiversiy We urn now o predicing proporional endemism (P E ) on he island In his sudy, we only consider endemism caused by evoluion [3,28], ie, species resuling from speciaion and ignore endemism caused by exincion on mainland and a oher sies where evoluion does no play a role Because speciaion adds endemic species o he island, exincion decreases he endemism, and migraion also decreases he endemism by dispersing endemic species from he island o he mainland, we can obain he number of endemics a ime +: S E( ) SE ( ) E D A SE ( ) I D A SE ( ) Then, he proporional endemism a ime is P E () S S E() I() DA ( ID A EDA DA) ( ID A EDA ) ( ID A EDA )[ ( ID A EDA DA ) ] ( ID A EDA ) ( ID A EDA DA) ( I D A E D A )[ (I D A E D A )] DA We find ha he proporion of endemic species increases wih ime (Figure 3), because more ime allows for inra-island speciaion o occur This paern agrees wih observaions ha high proporions of endemics are ofen associaed wih ancien islands [29,3] If ime increases o infiniy ( ), we can obain he proporional endemism of an island a equilibrium (P E ): DA E E / I ID A EDA P S S (3) Eq (3) shows ha he proporional endemism of an island a equilibrium is deermined by he raes of immigraion, exincion and speciaion per species, as well as by island physical feaures The proporional endemism is posiively correlaed o speciaion and negaively correlaed o immigraion and exincion [7] Eq (3) indicaes ha if, ie, he impac of disance on exincion is smaller han ha of speciaion a equilibrium, P E increases wih increasing isolaion (Figure 4), a paern observed in oceanic islands [25,3] However, if, proporional endemism increases wih increasing disance and approaches a Figure 3 Proporional endemism of he island over ime when S M =, I =8 3, E =5 3, =2 3, =5, =, =, =, =, = and A=25 Figure 4 Effecs of isolaion (D) and area (A) on he proporional endemism of he island when S M =, I =8 3, E =5 3, =2 3, =5, ==5, and ===

5 Chen X Y, e al Sci China Life Sci November (2) Vol54 No 59 IA ( ) maximum a D Eq (3) shows no E ( ) direc relaionship beween proporional endemism and island species richness However, island species richness is also deermined by migraion, exincion, speciaion, and island properies Therefore, proporional endemism co-varies wih island species richness, and a posiive relaionship can be observed beween hem [7] Proporional endemism is also relaed o island area If, proporional endemism increases coninuously wih increased area If, proporional endemism increases wih increasing area, approaches a maximum a A= ED ( ), and hen slowly bu coninuously I ( ) decreases Because he effec of area on immigraion is generally much larger han ha on speciaion, a maximum will be observed when area increases and oher parameers are fixed When area is small, exincion may lead o many species being los, including endemic species produced by speciaion; his effec decreases wih increasing area Meanwhile, immigraion may resul in a high proporion of new, non-endemic species, and his effec increases wih increasing area Therefore, i is reasonable o expec a criical area where P E is highes This resul is differen from MacArhur & Wilson s predicion ha P E migh be highes on large islands locaed in circular zones close o he ouermos dispersal ranges of he axa [] Alhough an island wih an area larger han his criical area will have a lowered proporional endemism, he decrease is no disinc (Figure 4) Therefore, a high proporion of endemism is generally expeced on large islands [6,9] 23 Implicaions for species richness and endemism on islands across developmen Many oceanic islands are volcanic in origin and experience a life cycle: a new volcanic island emerges from he sea, builds o a high cone-shaped form of maximal area and heigh, and hen becomes increasing disseced and eroded [3,28,32] To es our model, we predic he changes in immigraion, exincion, speciaion, and species richness on an island hroughou is exisence For simpliciy, we assume ha area increases linearly over ime and, afer reaching is maximum, decreases linearly o zero (Figure 5A), similar o he assumpion of Whiaker e al [3] As island area increases, he equilibrium diversiy, or poenial carrying capaciy [3], of he island increases and becomes highes a maximal area Realized species diversiy also increases wih increasing area, bu maximum species diversiy occurs afer maximal area has been reached and passed (Figure 5A) This paern is similar o he scenario described by Whiaker e al [3,33] In fac, he maximal value of realized Figure 5 Key raes and properies during he life of an island prediced by he generalized island biogeography model when S M, I =8 3, E =5 3, =2 3, D=25, =5, ==5, and === A, As in Whiaker e al [3], we consruced a hypoheical island and simplified he island area (black line) o increase linearly over ime (A=5, 6); i approaches a maximum a =6 followed by a linear decrease 3 3 over ime unil complee disappearance A, The equilibrium diversiy (green line) changes synchronously wih island area Realized species diversiy (red line) increases wih increasing area and approaches is maximum laer han does area Island endemism (blue line) increases wih increasing area unil he island has nearly disappeared B, Changes in he impacs of immigraion (purple line), exincion (brown line) and speciaion (green line) on species diversiy and proporional endemism (blue line) over ime on he same hypoheical island species diversiy occurs when i equals he equilibrium diversiy and is followed by a slow decrease in diversiy unil he island is close o disappearing back ino he sea (Figure 5A) Because our model has no considered ineracions among species, inherenly random exincion is he sole facor decreasing species diversiy Therefore, species diversiy decreases slowly even when he realized species diversiy is higher han equilibrium diversiy The final rapid decline is due o he island becoming oo small o suppor high species richness During island developmen, exincion and speciaion have similar rends, graphed by Whiaker e al [3,28], excep for a sharp increase in exincion and a sharp decrease in speciaion when he island approaches disappearance

6 6 Chen X Y, e al Sci China Life Sci November (2) Vol54 No (Figure 5B) Such a deceleraion of diversificaion over ime, led by increasing exincion raes due o drasic area declines, was observed in he woodlouse-huner spider genus Dysdera (Araneae, Dysderidae) on old volcanic islands [34] Generally, he impac of immigraion is also similar o ha described by Whiaker e al [3] However, a he earlies sages of island developmen, he immigraion rae is small, due o he very small area harboring low equilibrium diversiy, and hen increases rapidly o is maximum followed by a gradual decrease Similar o he speciaion rae, here is a sharp decrease in immigraion rae when he island approaches disappearance (Figure 5B) due o very limied island size During island developmen, he number of species eliminaed by exincion becomes greaer han ha added by immigraion and speciaion a he ime ha realized species diversiy becomes higher han he equilibrium diversiy of he island (Figure 5A and B) The number and percenage of endemic species increases wih ime, even afer he island approaches he maximal area and begins o erode, followed by a decrease when he island is eroded almos o disappearance (Figure 5A and B) Neverheless, our model indicaes ha islands ha are inermediae in age have he highes endemism The paern ha old islands generally have higher endemism han younger ones has been frequenly observed in archipelagos [29,3], bu he oldes islands have a decreased endemism due o loss of area by erosion [3] These resuls indicae ha, based on he generalized model, he prediced paerns of species richness, endemism and relaive conribuions of immigraion, speciaion and exincion on an oceanic island across is developmen are similar o empirical observaions [3,28] 3 Conclusion The developmen of a heoreical model combining ecological and evoluionary processes as well as island feaures is of cenral imporance o island biogeography Based on MacArhur and Wilson s model, Lomolino [5] graphed a riparie model of island biogeography as a general framework for undersanding he relaive roles of immigraion, exincion and speciaion in he mainenance of island species diversiy and why islands have high endemism Inra-island speciaion plays an imporan role in boh island species richness and endemism The conribuion of speciaion o local species diversiy may evenually exceed ha of immigraion under cerain condiions, depending on he speciaion and exincion raes per species and on island feaures We predic ha large islands have a high, bu no he highes, proporional endemism Furhermore, his model may predic changes in key raes, species diversiy and endemism across he life of an island, providing explanaions for he observed relaionships beween species richness or endemism and island feaures However, we should noe ha our model is based on a consan per species speciaion rae on he island, alhough hese raes are differen on differen islands For example, a burs of speciaion was found a he beginning of adapive radiaion and shorly hereafer [23] Neverheless, our model is an ideal saring poin for re-evaluaing he role of speciaion and re-analyzing available daa on island species diversiy, especially hose biased by he MacArhur-Wilson model We hank Rober J Whiaker, He FangLiang and wo anonymous reviewers for consrucive commens This work was suppored by he Naional Naural Science Foundaion of China (Gran No 38736), he Naional High Technology Research and Developmen Program of China (Gran No 27AA9Z432) and he 2 Projec of Eas China Normal Universiy MacArhur R H, Wilson E O An equilibrium heory of insular zoogeography Evoluion, 963, 7: MacArhur R H, Wilson E O The Theory of Island Biogeography Princeon: Princeon Universiy Press, Whiaker R J, Trianis K A, Ladle R J A general dynamic heory of oceanic island biogeography J Biogeogr, 28, 35: Wu J, Vanka J L Island biogeography: heory and applicaions In: Nierenberg W A, ed Encyclopedia of Environmenal Biology San Diego: Academic Press, Lomolino M V A call for a new paradigm of island biogeography Global Ecol Biogeogr, 2, 9: 6 6 Losos J B, Schluer D Analysis of an evoluionary species-area relaionship Naure, 2, 48: Wilson E O, Taylor R W An esimae of he poenial evoluionary increase in species densiy in he Polynesian an fauna Evoluion, 967, 2: 8 Darwin C The Origin of Species London: John Murray, Emerson B C, Kolm N Species diversiy can drive speciaion Naure, 25, 434: 5 7 Goldberg J, Trewick S A, Paerson A M Evoluion of New Zealand's erresrial fauna: a review of molecular evidence Philos T R Soc B, 28, 363: Kim S C, McGowen M R, Lubinsky P, e al Timing and empo of early and successive adapive radiaions in Macaronesia PLoS ONE, 28, 3: e239 2 Seppan S J, Zawadzki C, Heaney L R, e al Molecular phylogeny of he endemic Philippine roden Apomys (Muridae) and he dynamics of diversificaion in an oceanic archipelago Biol J Linn Soc, 23, 8: Ricklefs R E Esimaing diversificaion raes from phylogeneic informaion Trends Ecol Evol, 27, 22: Hubbell S P The Unified Neural Theory of Biodiversiy and Biogeography Princeon: Princeon Universiy Press, 2 5 Heaney L R Dynamic disequilibrium: a long-erm, large-scale perspecive on he equilibrium model of island biogeography Global Ecol Biogeogr, 2, 9: Brown J H, Lomolino M V Concluding remarks: hisorical perspecive and he fuure of island biogeography heory Global Ecol Biogeogr, 2, 9: Chen X Y, He F Speciaion and endemism under he model of island biogeography Ecology, 29, 9: Gilpin M E, Diamond J M Calculaion of immigraion and exincion curves from he species-area-disance relaion Proc Nal Acad Sci USA, 976, 73: He F, Gason K J, Connor E F, e al The local-regional relaionship: immigraion, exincion, and scale Ecology, 25, 86: Wu J, Vanka J L A sysem dynamics model of island biogeography Bull Mah Biol, 99, 53: Brown J H, Kodric-Brown A Turnover raes in insular biogeography: effec of immigraion on exincion Ecology, 977, 58:

7 Chen X Y, e al Sci China Life Sci November (2) Vol54 No 6 22 Roos M C, Kessler P J A, Gradsein S R, e al Species diversiy and endemism of five major Malesian islands: diversiy-area relaionships J Biogeogr, 24, 3: Gavriles S, Losos J B Adapive radiaion: conrasing heory wih daa Science, 29, 323: Kisel Y, Barraclough T G Speciaion has a spaial scale ha depends on levels of gene flow Am Na, 2, 75: Borges P A V, Horal J Time, area and isolaion: facors driving he diversificaion of Azorean arhropods J Biogeogr, 29, 36: Keppel G, Lowe A J, Possingham H P, e al Changing perspecives on he biogeography of he ropical Souh Pacific: influences of dispersal, vicariance and exincion J Biogeogr, 29, 36: Whiaker R J, Fernandez-Palacios J M Island Biogeography: Ecology, Evoluion, and Conservaion New York: Oxford Universiy Press, Whiaker R J, Trianis K A, Ladle R J, e al A general dynamic heory of oceanic island biogeography: exending he MacArhur-Wilson heory o accommodae he rise and fall of volcanic islands In: Losos J B, Ricklefs R E, MacArhur R H, eds The Theory of Island Biogeography Revisied Princeon: Princeon Universiy Press, Borges P A V, Brown V K Effec of island geological age on he arhropod species richness of Azorean pasures Biol J Linn Soc, 999, 66: Pereira H M, Proença V M, Vicene L, e al Does species diversiy really drive speciaion? Ecography, 27, 3: Gillespie R G, Roderick G K Arhropods on islands: colonizaion, speciaion, and conservaion Ann Rev Enomol, 22, 47: Price J P, Clague D A How old is he Hawaiian bioa? Geology and phylogeny sugges recen divergence Proc Roy Soc B Biol Sci, 22, 269: Whiaker R J, Ladle R J, Araújo M B, e al The island immauriy speciaion pulse model of island evoluion: an alernaive o he diversiy beges diversiy model Ecography, 27, 3: Macias-Hernandez N, Oromí P, Arnedo M A, e al Paerns of diversificaion on old volcanic islands as revealed by he woodlouse-huner spider genus Dysdera (Araneae, Dysderidae) in he easern Canary Islands Biol J Linn Soc, 28, 94: Open Access This aricle is disribued under he erms of he Creaive Commons Aribuion License which permis any use, disribuion, and reproducion in any medium, provided he original auhor(s) and source are credied