If threatened species go extinct, up to 10 Ma needed to return to today’s levels

It would take 50 million years (Ma) to recover the diversity of bird species lost

Large numbers of bird species went extinct in New Zealand after human colonization

Islands are at the frontline of the anthropogenic extinction crisis []. A vast number of island birds have gone extinct since human colonization [], and an important proportion is currently threatened with extinction []. While the number of lost or threatened avian species has often been quantified [], the macroevolutionary consequences of human impact on island biodiversity have rarely been measured []. Here, we estimate the amount of evolutionary time that has been lost or is under threat due to anthropogenic activity in a classic example, New Zealand. Half of its bird taxa have gone extinct since humans arrived [] and many are threatened [], including lineages forming highly distinct branches in the avian tree of life []. Using paleontological and ancient DNA information, we compiled a dated phylogenetic dataset for New Zealand’s terrestrial avifauna. We extend the method DAISIE developed for island biogeography [] to allow for the fact that many of New Zealand’s birds are evolutionarily isolated and use it to estimate natural rates of speciation, extinction, and colonization. Simulating under a range of human-induced extinction scenarios, we find that it would take approximately 50 million years (Ma) to recover the number of species lost since human colonization of New Zealand and up to 10 Ma to return to today’s species numbers if currently threatened species go extinct. This study puts into macroevolutionary perspective the impact of humans in an isolated fauna and reveals how conservation decisions we take today will have repercussions for millions of years.

New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene.

The Lost World of the Moa: Prehistoric Life of New Zealand.

Results

6 Worthy T.H.

Holdaway R.N. The Lost World of the Moa: Prehistoric Life of New Zealand. 13 Losos J.B.

Ricklefs R.E. Adaptation and diversification on islands. 14 Wallace A.R. Island Life: Or, The Phenomena and Causes of Insular Faunas and Floras, Including a Revision and Attempted Solution of the Problem of Geological Climates. 15 Wallis G.P.

Jorge F. Going under down under? Lineage ages argue for extensive survival of the Oligocene marine transgression on Zealandia. 14 Wallace A.R. Island Life: Or, The Phenomena and Causes of Insular Faunas and Floras, Including a Revision and Attempted Solution of the Problem of Geological Climates. 9 Gibb G.C.

England R.

Hartig G.

McLenachan P.A.

Taylor Smith B.L.

McComish B.J.

Cooper A.

Penny D. New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene. 10 Mitchell K.J.

Llamas B.

Soubrier J.

Rawlence N.J.

Worthy T.H.

Wood J.

Lee M.S.Y.

Cooper A. Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. 16 Mitchell K.J.

Wood J.R.

Llamas B.

McLenachan P.A.

Kardailsky O.

Scofield R.P.

Worthy T.H.

Cooper A. Ancient mitochondrial genomes clarify the evolutionary history of New Zealand’s enigmatic acanthisittid wrens. 6 Worthy T.H.

Holdaway R.N. The Lost World of the Moa: Prehistoric Life of New Zealand. 16 Mitchell K.J.

Wood J.R.

Llamas B.

McLenachan P.A.

Kardailsky O.

Scofield R.P.

Worthy T.H.

Cooper A. Ancient mitochondrial genomes clarify the evolutionary history of New Zealand’s enigmatic acanthisittid wrens. 17 Worthy T.H.

De Pietri V.L.

Scofield R.P. Recent advances in avian palaeobiology in New Zealand with implications for understanding New Zealand’s geological, climatic and evolutionary histories. 18 Trewick S.A.

Gibb G.C. Vicars, tramps and assembly of the New Zealand avifauna: a review of molecular phylogenetic evidence. 6 Worthy T.H.

Holdaway R.N. The Lost World of the Moa: Prehistoric Life of New Zealand. 9 Gibb G.C.

England R.

Hartig G.

McLenachan P.A.

Taylor Smith B.L.

McComish B.J.

Cooper A.

Penny D. New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene. 19 Wright T.F.

Schirtzinger E.E.

Matsumoto T.

Eberhard J.R.

Graves G.R.

Sanchez J.J.

Capelli S.

Müller H.

Scharpegge J.

Chambers G.K.

Fleischer R.C. A multilocus molecular phylogeny of the parrots (Psittaciformes): support for a Gondwanan origin during the cretaceous. 9 Gibb G.C.

England R.

Hartig G.

McLenachan P.A.

Taylor Smith B.L.

McComish B.J.

Cooper A.

Penny D. New Zealand passerines help clarify the diversification of major songbird lineages during the Oligocene. 20 Prum R.O.

Berv J.S.

Dornburg A.

Field D.J.

Townsend J.P.

Lemmon E.M.

Lemmon A.R. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. 10 Mitchell K.J.

Llamas B.

Soubrier J.

Rawlence N.J.

Worthy T.H.

Wood J.

Lee M.S.Y.

Cooper A. Ancient DNA reveals elephant birds and kiwi are sister taxa and clarifies ratite bird evolution. New Zealand’s biota is known for its evolutionary distinctiveness and unusual species composition []. Despite its origins as an ancient continental fragment, New Zealand has a distinctively insular character, leading Alfred Russel Wallace to declare that its “wonderfully isolated” biota resembles that of oceanic islands []. A remarkable feature of New Zealand is that, unlike other large landmasses, its vertebrate fauna has long been dominated by birds, many of which form highly distinct evolutionary lineages []. The Quaternary avifauna of New Zealand—often called a “land of birds”—includes examples such as a giant nocturnal parrot (kakapo), the flightless moa (Dinornithiformes), and the country’s national bird, the kiwi (Apterygidae) []. A characteristic feature of New Zealand is the taxonomic and ecological uniqueness of its bird clades, generally attributed to its prolonged geographical isolation and/or ancient Gondwanan heritage []. Compared to other similar-sized landmasses, there are relatively few species of land (non-aquatic) birds, most of which are found nowhere else []. The country harbors several groups forming deep isolated phylogenetic branches [], including the sister clade of parrots (Strigopoidea) [] and passerines (New Zealand wrens, Acanthisittidae) [], and two endemic clades of palaeognaths (kiwi and moa), the sister group to all other birds [].

21 Seersholm F.V.

Cole T.L.

Grealy A.

Rawlence N.J.

Greig K.

Knapp M.

Stat M.

Hansen A.J.

Easton L.J.

Shepherd L.

et al. Subsistence practices, past biodiversity, and anthropogenic impacts revealed by New Zealand-wide ancient DNA survey. 22 McDowall R.M. Process and pattern in the biogeography of New Zealand–a global microcosm?. 23 Wilmshurst J.M.

Anderson A.J.

Higham T.F.G.

Worthy T.H. Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat. 24 Jacomb C.

Holdaway R.N.

Allentoft M.E.

Bunce M.

Oskam C.L.

Walter R.

Brooks E. High-precision dating and ancient DNA profiling of moa (Aves: Dinornithiformes) eggshell documents a complex feature at Wairau Bar and refines the chronology of New Zealand settlement by Polynesians. 7 Holdaway R.N. Introduced predators and avifaunal extinction in New Zealand. 25 Holdaway R.N.

Worthy T.H.

Tennyson A.J.D. A working list of breeding bird species of the New Zealand region at first human contact. 7 Holdaway R.N. Introduced predators and avifaunal extinction in New Zealand. 26 Duncan R.P.

Blackburn T.M. Extinction and endemism in the New Zealand avifauna. 1 Whittaker R.J.

Fernández-Palacios J.M.

Matthews T.J.

Borregaard M.K.

Triantis K.A. Island biogeography: Taking the long view of nature’s laboratories. 2 Steadman D.W. Extinction and Biogeography of Tropical Pacific Birds. 4 Blackburn T.M.

Cassey P.

Duncan R.P.

Evans K.L.

Gaston K.J. Avian extinction and mammalian introductions on oceanic islands. 8 Robertson H.A.

Baird K.

Dowding J.E.

Elliott G.P.

Hitchmough R.A.

Miskelly C.M.

McArthur N.

O’Donnell C.F.J.

Sagar P.M.

Scofield R.P.

et al. Conservation status of New Zealand birds, 2016. The unique avifauna of New Zealand is an excellent example to study the role of human occupancy in disturbing natural communities []. New Zealand was the last major habitable land area to be settled by humans []. Polynesian Maori arrived about 700 years ago and Europeans have been present for 200–300 years []. Although all bird species known from Late Pleistocene deposits survived into the period of first human occupation, nearly half were driven to extinction during the following years of settlement []. The avifauna of New Zealand suffered one of the largest waves of extinction documented. The high incidence of flightlessness (over a third of land bird species upon human arrival), large body size, and behavioral naiveté have contributed toward susceptibility of native birds to hunting, introduced species and land-use change []—a recurring pattern in most isolated islands worldwide []. Despite innovative conservation efforts in the country over the last 50 years, over 30% of extant species remain threatened with extinction, and nearly two thirds could be under threat in the future [].

While the impact of humans on New Zealand’s extinct and threatened bird species numbers is relatively well understood, little is known about the long-term macroevolutionary impact of anthropogenic extinction. In other words, how far have humans perturbed this unique and isolated biological assembly from its natural state? And how deep will the evolutionary impact be if currently threatened species go extinct? Would diversity quickly return to natural levels if left to evolve under its natural trajectory of colonization and speciation (with no further human-induced extinctions)? Here, we address these questions for the first time in an insular avifauna.

12 Valente L.M.

Phillimore A.B.

Etienne R.S. Equilibrium and non-equilibrium dynamics simultaneously operate in the Galápagos islands. 53 Valente L.

Phillimore A.

Etienne R.S. Using molecular phylogenies in island biogeography: it’s about time. 53 Valente L.

Phillimore A.

Etienne R.S. Using molecular phylogenies in island biogeography: it’s about time. 54 Valente L.

Etienne R.S.

Dávalos L.M. Recent extinctions disturb path to equilibrium diversity in Caribbean bats. 12 Valente L.M.

Phillimore A.B.

Etienne R.S. Equilibrium and non-equilibrium dynamics simultaneously operate in the Galápagos islands. We used the DAISIE (Dynamic Assembly of Islands through Speciation, Immigration, and Extinction) [] framework to estimate pre-human (i.e., natural) rates of species accumulation in New Zealand. Its maximum likelihood implementation allows parameters of colonization, speciation via cladogenesis (i.e., when one species splits into two new species) and anagenesis (i.e., when a new species is formed without lineage splitting) and natural extinction to be estimated based on the colonization and branching times for an entire community on an insular system. DAISIE has been shown to estimate these rates with little bias []. The rate of natural extinction—i.e., the background rate at which species go extinct from the system in the absence of humans—is usually well estimated in this framework []. The method uses information from the distribution of branching times within island radiations in combination with additional information from the separate colonization times. In its parameterization of extinction, DAISIE assumes and accounts for the fact that there may have been several lineages of taxa that were present on the island before humans but which went completely extinct due to natural causes, leaving no extant descendants (and often, no fossils). We did not test for non-homogeneous rates of colonization, speciation, and extinction (e.g., as in []) because we do not have an a priori hypothesis of different rates for a specific group and because we are interested in average rates in New Zealand.

We extended DAISIE to accommodate that most New Zealand bird radiations are very old and have no extant close relatives. The method was extended by allowing for a colonization event to have occurred any time between the stem age and the crown age of a New Zealand radiation (see STAR Methods ). We implemented the new method in a new version of the R package DAISIE. We then fitted several DAISIE models to the phylogenetic data, assuming that New Zealand has existed as a continuously habitable isolated insular system for the past 52 Ma (but see STAR Methods for a sensitivity analysis of this assumption). Under the best supported macroevolutionary model of bird species accumulation in New Zealand (model M1, Table S2 ), bird species colonized at a rate of 4.7 events every million years (Ma), while new species originated through both cladogenesis and anagenesis at a rate of 0.125 and 0.33 speciation events per lineage per Ma, respectively, and went extinct through natural extinction at a rate of 0.19 extinction events per Ma. Because extinction exceeds the rate of cladogenesis, avian biodiversity on New Zealand is maintained by colonization; i.e., New Zealand constitutes a macroevolutionary sink for birds. Simulations of the model reveal a good fit to the data ( Figure S1 ).

54 Valente L.

Etienne R.S.

Dávalos L.M. Recent extinctions disturb path to equilibrium diversity in Caribbean bats. 55 Davis M.

Faurby S.

Svenning J.-C. Mammal diversity will take millions of years to recover from the current biodiversity crisis. 56 Triantis K.A.

Economo E.P.

Guilhaumon F.

Ricklefs R.E. Diversity regulation at macro-scales: species richness on oceanic archipelagos. We estimated how long it would take on average for bird species diversity in New Zealand to return to a given level using a recently developed island evolutionary return time metric []. This metric uses the information on the natural rates of species assembly for a given insular system (estimated using DAISIE) and measures how long it would take for species diversity on that island to increase to a predetermined level (often pre-human levels) by simulating under those same rates into the future. This metric is calculated for each island system (e.g., island, lake, archipelago) and is thus island rather than lineage centric and can allow for the macroevolutionary impact of humans on different islands to be compared. The evolutionary return time differs from methods that measure the amount of lost phylogenetic diversity [] because the latter approaches do not take into account the specific local biogeographical processes that are taking place on each island (and which differ with island characteristics such as area and isolation []). We studied three scenarios: (1) the return from current diversity to pre-human and pre-European number of species; (2) the return from diversity that would remain if currently threatened species (critically endangered, endangered, and vulnerable) became extinct back to current number of species; (3) the return from diversity that would remain if currently threatened as well as near-threatened species became extinct back to the current number of species.