Journal of Biogeography (J. Biogeogr.) (2014)
ORIGINAL
ARTICLE
Quantifying surface-area changes of
volcanic islands driven by Pleistocene
sea-level cycles: biogeographical
implications for the Macaronesian
archipelagos
Kenneth F. Rijsdijk1*, Tom Hengl2, Sietze Norder1, R€
udiger Otto3,
5, Heriberto L
Brent C. Emerson4, Sergio P. Avila
opez4, E. Emiel van Loon1,
6
3
Even Tjørve and Jose Marıa Fernandez-Palacios
1
Computation GeoEcology Group, Institute for
Biodiversity and Ecosystem Dynamics &
Institute for Interdisciplinary Studies,
University of Amsterdam, Sciencepark 904,
1098 XH Amsterdam, The Netherlands,
2
ISRIC–World Soil Information, 6700 AJ
Wageningen, The Netherlands, 3Instituto
Universitario de Enfermedades Tropicales y
Salud P
ublica de Canarias (IUETSPC),
Universidad de La Laguna, Tenerife, Canary
Islands, Spain, 4Island Ecology and Evolution
Research Group, IPNA-CSIC, 38206 La
Laguna Tenerife, Canary Islands, Spain,
5
Faculdade de Ci^encias da Universidade do
Porto and CIBIO, Centro de Investigacß~ao em
Biodiversidade e Recursos Geneticos, InBIO
Laboratorio Associado, Polo dos Acßores and
Departamento de Biologia, Universidade dos
Acßores, 9501–801 Ponta Delgada, Acßores,
Portugal, 6Lillehammer University College,
2604 Lillehammer, Norway
*Correspondence: Kenneth F. Rijsdijk,
Computation GeoEcology Group, Institute for
Biodiversity and Ecosystem Dynamics &
Institute for Interdisciplinary Studies,
University of Amsterdam, Sciencepark 904,
1098 XH Amsterdam, The Netherlands.
E-mail: [email protected]
ª 2014 John Wiley & Sons Ltd
ABSTRACT
Aim We assessed the biogeographical implications of Pleistocene sea-level fluctuations on the surface area of Macaronesian volcanic oceanic islands. We
quantified the effects of sea-level cycles on surface area over 1000-year intervals.
Using data from the Canarian archipelago, we tested whether changes in island
configuration since the late Pleistocene explain species distribution patterns.
Location Thirty-one islands of four Macaronesian archipelagos (the Azores,
Madeira, the Canary Islands and Cape Verde).
Methods We present a model that quantifies the surface-area change of volcanic islands driven by fluctuations in mean sea level (MSL). We assessed statistically whether Canarian islands that were merged during sea-level lowstands
exhibit a significantly higher percentage of shared (endemic) species than other
comparable neighbouring islands that remained isolated, using multimodel
comparisons evaluated using the Akaike information criterion (AIC).
Results Each Macaronesian island exhibited a unique area-change history. The
previously connected islands of Lanzarote and Fuerteventura share significantly
more species of Insecta than the similarly geographically proximate island pair
of La Gomera and Tenerife, which have never been connected. Additionally,
Lanzarote and Fuerteventura contain the highest percentage of two-island
endemic Plantae species compared with all other neighbouring island pairs
within the Canaries. The multimodel comparison showed that past connectedness provides improved explanatory models of shared island endemics.
Main conclusions Pleistocene sea-level changes resulted in abrupt alterations
in island surface areas, coastal habitats and geographical isolation, often within
two millennia. The merging of currently isolated islands during marine lowstands may explain both shared species richness and patterns of endemism on
volcanic islands. Currently, the islands are close to their long-term minimum
surface areas and most isolated configurations, suggesting that insular biota are
particularly vulnerable to increasing human impact.
Keywords
Canary Islands, connectivity, extinction, island biogeography, Macaronesia,
multiple-island endemics, Pleistocene sea level, sea-level changes, target effect,
volcanic islands.
http://wileyonlinelibrary.com/journal/jbi
doi:10.1111/jbi.12336
1
K. F. Rijsdijk et al.
INTRODUCTION
The biogeographical implications of insular dynamics as a
result of Pleistocene sea-level fluctuations have long been
recognized, but research has been mainly, although not
exclusively, focused on continental shelf settings and landbridge islands (e.g. Mayr, 1944; Diamond, 1972; Wilcox,
1978; Heaney, 1984, 1986; Richman et al., 1988; Moody,
2000; Qian & Ricklefs, 2000; Price & Elliott-Fisk, 2004). Qian
& Ricklefs (2000) suggested that cyclical fragmentation
induced by sea-level cycles has promoted allopatric speciation of plants. They explain the higher species richness in
temperate eastern Asia compared with North America as
being a consequence of higher continental sea-floor variability in the former region. Palaeogeographical reconstructions
in Southeast Asia (e.g. Mayr, 1944; Voris, 2000) show that,
during the last ice age, continents extended further seaward.
Shallow shelf seas were exposed, previously isolated islands
were connected to the mainland, and all islands had larger
subaerial surface areas (referred to from now on simply as
surface area). At the end of the last glacial period, c. 16 ka,
the mean sea level (MSL) rose from c. –120 m to approach
its current level (Fig. 1, point D; Cutler et al., 2003). Consequently, inland shelf seas were flooded, islands were formed
by isolation from continents and all islands were reduced in
surface area, ultimately resulting in the surface area and
archipelago configurations that we know today. Several
Sea level
(m)
F
0
A
B
E
-20
-40
-60
C
-80
D
-100
-120
0
20
60
40
80
Thousand years ago
100
120
Figure 1 Global sea-level change during the last 120 kyr.
Generalized mean sea level (MSL) reconstruction from 120 ka
based on Camoin et al. (2004). Regions that are uncertain in
Camoin et al. (2004) were interpolated linearly. At point A,
Eemian interglacial sea levels were 10 m higher than today; at
point B, sea levels fell with the onset of the glacial epoch, and
warmer periods (interstadials) alternating with colder periods
(stadials) led to sea-level fluctuations between –20 and –60 m; at
point C, there was then a period of relative stability, although
this may be an artefact of data sampling. Point D marks the
extreme sea-level fall during the Late Glacial Maximum (LGM);
point E marks the rapid sea-level rise at the end of the LGM;
and point F marks the stabilization of sea levels at present-day
levels.
2
authors have suggested that sea-level fluctuations must have
caused variations in immigration and extinction by changing
island carrying capacities and isolation, not only by the
repeated submersion and re-appearance of land bridges but
also by the increase and reduction of island surface areas
(e.g. Diamond, 1972; Wilcox, 1978; Richman et al., 1988;
Mayr & Diamond, 2001; Louys et al., 2007; Whittaker et al.,
2010; Fernandez-Palacios et al., 2011; Avila,
in press). Moreover, sea-level changes would have affected migration rates
through distance and target area effects (e.g. MacArthur &
Wilson, 1967, p. 127) derived from changes in island surface
areas, inter-island distances and distances to continents. Previously submerged seamounts that emerged because of sealevel falls would have opened up new dispersal routes and,
thus, increased immigration probabilities within or among
archipelagos, as well as between archipelagos and continents
(Garcıa-Talavera, 1999; Avila,
2000; Avila
& Malaquias, 2003;
Avila
et al., 2009; Warren et al., 2010; Fernandez-Palacios
et al., 2011; Ali & Aitchison, 2014). It is biogeographically
relevant to point out that the present-day sea level is anomalously high for the Quaternary period, considering that the
mean for the last 0.9 Myr has been about 60 m lower than
the present MSL. During the last 0.9-Myr period, sea-level
cycles have been similar in amplitude, asymmetry (long glacial periods) and periodicity (Ruddiman, 2003). Sea-level
cycles with an approximate 100-kyr periodicity have resulted
from ice ages lasting c. 90 kyr alternating with interglacials
lasting c. 10 kyr. These cycles coincide with observed low
and high sea-level stands, respectively (e.g. Lambeck et al.,
2002; Bintanja et al., 2005). During the glacial maximum,
when ice sheets were at their largest extent, sea levels fell to
as much as –120 m MSL, whereas they rose to a maximum
of around +10 m MSL during the interglacial periods (Cutler
et al., 2003; Bintanja et al., 2005).
The last sea-level cycle (glacial–interglacial period) commenced with a relatively short highstand lasting 10 kyr
(Fig. 1, point A). Then, during the early interglacial (120–70
ka), sea levels fell and fluctuated between –20 and –60 m
MSL (Fig. 1, point B). In the following 40 kyr, sea levels
dropped rapidly by 10.6 m kyr 1 to –80 m MSL, followed
by an additional fall to below –120 m MSL during the glacial
maximum (40–16 ka) (Fig. 1, points C and D; Cutler et al.,
2003). Consequently, from about 76 to 16 ka, when sea levels
were at their lowest (between –80 and –120 m MSL: Fig. 1,
point D), the Macaronesian islands achieved their largest
surface areas and additional seamounts were also emergent
(Garcıa-Talavera, 1999; Avila,
2000; Avila
& Malaquias, 2003;
Fernandez-Palacios et al., 2011). During the subsequent sealevel rise that began c. 16 ka, islands rapidly decreased in
surface area (Fig. 1, point E) as the sea level rose fast, by
5–15 m kyr 1, up until 7 ka, when the rise decelerated to
c. 1 m kyr 1 (Fig. 1, point F). Global sea level stabilized and
reached its present level c. 2500 years ago (Zinke et al., 2001;
Camoin et al., 2004). Hence, for volcanic (hotspot) oceanic
islands, the concerted action of sea-level rise from c. 16 ka,
and global warming during a glacial–interglacial transition,
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
has led to habitat surface-area reductions for many and perhaps most terrestrial species. Climate warming has caused
major upward elevational shifts of habitats and biomes globally (de Boer et al., 2013; Hooghiemstra et al., 2014). These
combined effects may have resulted in a reduction of both
lowland and upland habitat areas and a reduction of carrying
capacity for some biota.
Present-day seamounts as low as –120 m MSL, which
acted as stepping-stones during the glacial period, such as
those between Iberia and Madeira and between the Canary
Islands and Africa (Avila
& Malaquias, 2003; Gofas, 2007;
Fernandez-Palacios et al., 2011), became submerged as sea
levels rose. In addition, some islands became fragmented, as
was the case with the Canarian palaeo-island of Mahan,
which gave rise to Lanzarote, Fuerteventura and several islets
(Garcıa-Talavera, 1999; Fernandez-Palacios et al., 2011).
Consequently, the ranges of some species within Mahan
became fragmented, resulting in a reduction or cessation of
gene flow among vicariant populations.
Whittaker et al. (2010) have suggested that the observed
disjunct distribution of some multiple-island endemics
(MIEs) may be the result of localized vicariance caused by
the recent sea-level rise dividing formerly continuous islands;
thereby single-island endemics (SIEs) of previously united
islands became MIEs. The absence of estimates of the magnitude of insular surface-area changes, and the rates, timings
and durations of sea level-driven insular changes, prevents
quantitative biogeographical assessments of such theoretical
speculation. However, as global sea-level fluctuations from
120 ka, and in particular from 16 ka, have been reconstructed in detail (Fig. 1; Zinke et al., 2001; Cutler et al.,
2003; Camoin et al., 2004; Peltier & Fairbanks, 2006), the
effects of sea-level change on islands and archipelagos can be
quantified.
Using the last sea-level cycle, we have developed a palaeobio-island geographic information system (GIS) model
(p-BIG model) to quantify insular changes in surface area
and isolation, in order to assess the biogeographical implications of sea-level changes in archipelago configurations of
volcanic oceanic islands. We selected four Macaronesian
archipelagos in the Atlantic Ocean (Fig. 2), comprising 31
islands that form representative examples of the ontogenetic
range (< 0.5 Ma, > 20 Ma) of volcanic islands (FernandezPalacios et al., 2011). Eleven of these islands, with surface
areas larger than 4 km2, were connected to other islands during the Pleistocene. We then analysed the palaeo-history of
Fuerteventura and Lanzarote within the Canary Islands as an
illustrative example of how species richness may be affected
by sea level-induced surface-area change, as they were united
as a single island during sea-level lowstands, forming the palaeo-island Mahan. We hypothesized that islands that were
united during the Pleistocene will share more native species
than islands with a similar inter-island distance that have
remained isolated from each other. We also hypothesized
that if contemporary islands were more frequently connected
than isolated, they will exhibit the biogeographical properties
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
The Azores
Spain
Madeira
Atlantic Ocean
The Canary Islands
Africa
N
Cape Verde
500 km
Figure 2 Location of the Macaronesian archipelagos in the
Atlantic Ocean.
of a single island, sharing more endemic species than
islands that were not connected. To address these two
hypotheses, we used p-BIG to quantify the palaeo-surface
change of Mahan, to infer the duration of the connection
of Fuerteventura and Lanzarote, and to estimate the timing
of their isolation from each other. Using both insect and
plant distribution data, we then tested the prediction that,
because of their history of geographical union, species sharing will be higher between Lanzarote and Fuerteventura
compared with the similarly geographically proximate
islands of La Gomera and Tenerife. Using only plant species
distribution data, we further tested the prediction that there
are more shared MIEs between Lanzarote and Fuerteventura
compared with other island pairs within the Canaries that
have always been isolated. We discuss some important
biogeographical implications of sea-level change and the
potential to implement the model to extend the general
dynamic theory of oceanic island biogeography (e.g.
Whittaker et al., 2008).
MATERIALS AND METHODS
Modelling area change
To obtain contemporary island surface areas for Macaronesian islands, we used the present-day island boundary polygons of the island administrative boundaries from the Global
Administrative Areas database (GADM; Hijmans et al.,
2010). Missing island boundaries were digitized manually
from the high-resolution Ikonos images of Google Earth
(Patterson, 2007). In GIS terms, an island is defined as a collection of closed polygons representing land mass (Fig. 3a).
The minimum area for a given polygon to be a separate
island is 3 km2 (see Appendix S1 in Supporting Information). In order to derive distances from oceanic islands to
3
K. F. Rijsdijk et al.
(a)
Island
Polygon #3
<3
km
Minimum
distance
> 5 km
Gravity point
Po
lyg
Po
lyg
on
on
Continental
landmass
#1
#2
(b)
DEM
Island boundaries
Area
Sea-level curve
Buffer
Distance
Figure 3 Island definition and work flow. (a) Island definition.
In order to model surface changes of islands, it is crucial to
employ a morphometric definition of an island that can be used
in an algorithm. Here an island is considered to be a separate
entity when, at the current mean sea level (MSL), the area of its
bounding box is larger than 3 km2, the distance of its gravity
point to a continent is larger than 5 km, and its minimum
boundary distance to another island or continent is larger than
3 km. See Appendix S1 for a complete description of island
classification. (b) Work flow. Flow diagram with processing
steps for calculating distance and area. These steps are
performed for each island per 1 kyr from 120 ka. The resulting
area and distance maps are used to calculate island indices.
DEM, digital elevation model.
the nearest continent, we used the World Vector Shoreline
dataset at a scale of 1:250,000 to construct a grid of closest
distances from points (islands) to continents (Wessel &
Smith, 1996; see Appendix S1). The distance to closest island
as a grid was derived iteratively for each island using buffer
distance operations in the GIS software (System for Automated Geoscientific Analyses, saga gis 2.0.8; http://www.
saga-gis.org/). We merged a terrestrial digital elevation model
(DEM), based on the Shuttle Radar Topography Mission
(SRTM) data (http://dds.cr.usgs.gov/srtm/version2_1/SRTM30/),
with a detailed bathymetric model (Becker et al., 2009), both
at a 1-km2 resolution (data set available from http://www.
worldgrids.org/). This merged DEM model was used to calculate the extent of a given palaeo-island at various sea-level
heights (Fig. 3b). For p-BIG, we used the free and opensource software R for statistical computing (R Core Team,
2012), in combination with the OSGeo software FWTools
(http://fwtools.maptools.org/) and saga gis (see Appendix
S2). saga gis was used for manipulation and calculations
within spatial grids, while R was the central programming
environment (Hengl, 2009). The link between GIS and R
operations was established via various R libraries (rsaga,
rodbc, rgdal) (Bivand et al., 2008). p-BIG produces maps
of the palaeo-extent of islands and palaeo-configurations of
the four archipelagos of Macaronesia for the last sea-level
cycle (Fig. 1) involving 120 time steps with intervals of 1
kyr. The resulting maps were used to construct island indices
that reflected the change in island surface area and archipelago configuration.
Comparisons of shared species and two-island
endemics
To demonstrate the utility of our model, we present an illustrative example based on available, suitable, species richness
data (n > 500) for Insecta and Plantae on Canarian islands
(see Appendix S3 for our sampling rationale). Statistical
analyses were carried out in R (see Appendix S2 for script
and data).
We performed two analyses of shared species, comparing
Lanzarote and Fuerteventura with the islands of La Gomera
and Tenerife. The first analysis used the entire island fauna,
while the second analysis was restricted to fauna within an
elevational range of 0–500 m MSL (Table 1). The second
analysis allowed for a more meaningful comparison between
Fuerteventura (807 m) and Lanzarote (671 m) (low-elevation
islands), and Tenerife (3718 m) and La Gomera (1489 m)
(high-elevation islands), because it excluded higher elevational species that are particular to Tenerife and La Gomera.
Table 1 Number and percentage of insect species shared on Tenerife and La Gomera (TF–GO) and Lanzarote and Fuerteventura
(LZ–FV). The number of species shared between two islands is indicated by n1&2 and the total number of species on both islands is
indicated by (n1+n2). In all cases, the percentages for island pair LZ–FV are significantly higher than for TF–GO (P < 0.001).
Insecta
Coleoptera
< 500 m
Whole island
< 500 m
Whole island
Island pairs
n1&2/(n1+n2)
%
n1&2/(n1+n2)
%
n1&2/(n1+n2)
%
n1&2/(n1+n2)
%
TF–GO
LZ–FV
P-value
1444/4135
765/1671
< 0.001
34.9
45.8
999/4135
631/1671
< 0.001
31.5
41.2
462/1357
300/561
< 0.001
34.1
53.5
359/1357
225/561
< 0.001
33.6
45.0
4
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
Analyses used Insecta (n = 5806) and Coleoptera (n = 1918)
data from the Canary Islands government biodiversity database (http://www.biodiversidadcanarias.es/; see Appendix S3)
for the islands of Lanzarote, Fuerteventura, Tenerife and La
Gomera. For both faunal groups, we compared the proportion of shared species between Lanzarote and Fuerteventura
and between La Gomera and Tenerife, and tested the null
hypothesis that the proportion of shared species is the same
for the two island pairs against the one-sided alternative
hypothesis that the proportion is greater on the island pair
that has been formerly united as a single island.
For Plantae, we use endemic species data (n = 544) from
eight geographically proximate island pairs within the Canary Islands with Akaike information criterion (AIC)-based
multimodel comparisons, to test whether past connectedness
is a significant predictor for shared island endemics. We
selected species representatives for lowland habitats from
coastal scrub and thermophilous woodland associations. The
correlation between SIEs and MIEs exclusive to an island
pair (2MIEs) was calculated for both modern Fuerteventura
and Lanzarote, and for the palaeo-island Mahan, to test the
prediction that including the connected palaeo-islands as a
predictor should provide better model fitting. Data for SIEs
(n = 271), MIEs (n = 136) and 2MIEs (n = 72) of coastal
scrub and thermophilous woodland species were compiled
from Arechavaleta et al. (2010) and classified by Zobel et al.
(2011) as lowland species. We formulated seven a priori linear models that might explain the number of 2MIEs
between island pairs: (1) distance (D) between islands,
including both present-day and Pleistocene minimum distances; (2) SIE; (3) connection (whether islands were
merged or not); (4) distance and SIE; (5) distance and connection; (6) SIE and connection; and (7) distance, SIE and
connection.
We subsequently evaluated, through multimodel comparison based on AICc (AIC with a correction for finite sample
sizes), which of these models were most consistent with the
observed data (Burnham & Anderson, 2002).
RESULTS
Morphometric results
With sea levels rising from –120 m MSL to present-day levels
during the Last Glacial Maximum (LGM; 26–19 ka; Fig. 1,
point D), most islands of the Azores were reduced in surface
area by between 20% and 50% (Fig. 4a). The islands of Faial
(173 km2) and Pico (444 km2) were united for a period of
c. 16 kyr between 30 and 14 ka to form Laurinsula, an island
of c. 800 km2 (the name Laurinsula is derived from laurel
forests that are believed to have dominated the landscape at
that time). These two islands were also connected between
57 and 43 ka and 72 and 66 ka (except for a short interval
around 70 ka).
Madeira (742 km2) was > 50% more extensive in surface
area during the LGM, reaching 1256 km2 (Fig. 4b), and was
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
connected to Desertas (Ilheu de Ch~ao, Deserta Grande and
Bugio, together constituting 14 km2) during the LGM
between 23 and 18 ka. However, within a single millennium,
Desertas was abruptly separated again from Madeira, around
18 ka. Between 72 and 13 ka, Porto Santo (today 43 km2)
was about five times larger than at present (reaching
240 km2 during the LGM).
The most substantial event in the Canary Islands (Fig. 4c)
took place between 77 and 9 ka, when the islands of Fuerteventura (1677 km2) and Lanzarote (850 km2), together with
the islets located north of Lanzarote (Alegranza, Monta~
na
Clara and La Graciosa) and north of Fuerteventura (Isla de
Lobos), were merged into a single larger island (Mahan) with
a surface area of c. 5000 km2. North of the western tip of
Mahan, some 15 km from its coast, the present-day seamount Amanay emerged during glacial periods, with an area
of c. 200 km2 and an elevation of c. 100 m, during the
LGM. The distance between Fuerteventura and Gran Canaria
increased from 55 km during the LGM to 87 km at present.
The distance from the African coast to Mahan was only
56 km during the LGM, compared with the 96 km separating contemporary Fuerteventura and the Saharan coast. Also
noteworthy for the Canaries is that, during the LGM, the
island of La Gomera (373 km2) had nearly twice its current
surface area, whereas Gran Canaria (1574 km2) was 1.6 times
larger than today.
The islands of Cape Verde experienced the most
extreme surface-area and configuration changes among the
Macaronesian archipelagos in the last sea-level cycle
(Fig. 4d). Between 74 and 13 ka, four windward islands
(S~ao Vicente, Santa Luzia, Ilheu Branco and Ilheu Raso)
were united to form a large island that achieved a surface
area of approximately 830 km2 during the LGM. This
island was less than 5 km from Santo Ant~ao (currently it
is 12 km). The distance between the islands of S~ao Nicolau and Santo Ant~ao is currently c. 75 km, but during the
LGM this distance was effectively reduced to less than
15 km because of the unification of the four windward
islands, which acted as a single stepping-stone located
between Santo Ant~ao and S~ao Nicolau. The island of Boa
Vista (632 km2) was, on average, 3.5 times larger than
today between 72 and 14 ka (with a maximum surface
area of c. 2750 km2 during the LGM). During this period,
the island of Maio (today 273 km2) was more than
850 km2, and the distance from Maio to Boa Vista was
reduced to less than 7.5 km compared with the present
distance of 77 km. In many cases, the periods of surfacearea reduction and increase tended to be abrupt. For
instance, Boa Vista (Cape Verde), Fuerteventura (Canary
Islands) and Desertas (Madeira) all changed surface area
3–10-fold within 1 or 2 kyr after c. 15 ka.
Shared species and two-island endemics
The proportion of shared Insecta and Coleoptera species between Fuerteventura and Lanzarote (Fig. 4c) is
5
K. F. Rijsdijk et al.
(a)
The Azores
Corvo
Island area
2
(km )
Flores
Graciosa
Sao Jorge Teirceira
Faial
Lau
Sao Miguel
rins
ula Pico
Sao Miguel
Pico
Teirceira
Sao Jorge
Faial
Flores
Santa Maria
Graciosa
Corvo
Santa Maria
N
100 km
Thousand years ago
(b)
Madeira
Island area
(km2)
Porto Santo
Madeira
Madeira
Desertas
N
50 km
Selvagens
Porto Santo
Desertas
Selvagens
Thousand years ago
Island area
(km2)
The Canaries
(c)
Lanzarote
Lanzarote
Fuerteventura
Mahan
La Palma
Tenerife
t
Amanay
as
Gran Canaria
co
La Gomera
Fuerteventura
Tenerife
Fuerteventura
Gran Canaria
Af
ric
an
El Hierro
Lanzarote
La Palma
La Gomera
El Hierro
N
100 km
Thousand years ago
(d)
Island area
(km2)
Cape Verde
Santo Antão
Boavista
São Vicente
Sal
Santa Luzia
São Nicolau
Ilhéu Branco
Ilhéu Raso
Boavista
Maio
Santiago
Maio
Sal
N
Fogo
Brava
Brava
Santiago
Santo Antão
Boavista
Fogo
São Nicolau
São Vicente
Santa Luzia
100 km
Thousand years ago
Figure 4 Surface change maps of (a) the Azores, (b) Madeira, (c) the Canary Islands and (d) Cape Verde. Left panels: the light-grey
areas represent the current island area, the dark-grey areas represent the maximum extensions of islands during the Last Glacial
Maximum (LGM) sea-level lowstand (120 m below the current level). Names in grey are palaeo-islands that emerged or were united
during the last glacial period. Right panels: absolute island area changes for Macaronesian islands from 120 ka. Where the lines overlap,
the islands are united.
6
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
approximately 10% higher than that between Tenerife and
La Gomera (Table 1). This pattern occurs for the taxa occurring across the entire elevational range of each island, as well
as for species only occurring lower than 500 m. In all four
analyses (Insecta, Coleoptera, entire elevational range, lowelevation species only), the differences between the proportions were highly significant (P < 0.001) (Table 1).
Concerning the prediction for 2MIEs for plant species,
Lanzarote and Fuerteventura were found to contain the highest percentage of 2MIEs (Table 2), suggesting that, from a
plant evolutionary perspective, they represent or are equivalent to a single island. There was a significant correlation
between SIEs and 2MIEs when considering Lanzarote and Fuerteventura as the single palaeo-island Mahan (r2 = 0.6561,
P < 0.001) (Fig. 5), whereas there was no significant correlation when considering Lanzarote and Fuerteventura separately
(r2 = 0.0625, P = 0.3484) (Fig. 5). The multimodel comparison showed that, for lowland Plantae, past connectedness
was, in combination with SIEs and distance, a very significant
variable explaining 2MIEs (Table 3). Including LGM distances as a predictor yielded similar models as present-day
distances, which was not surprising as these distances correlated strongly with each other (r2 = 0.7707, P < 0.001).
DISCUSSION
Connectivity and surface-area change
The volcanic archipelagos of Macaronesia illustrate how
Quaternary sea-level cycles have reconfigured island surface
areas within archipelagos. It is crucial to recognize that, during most of the last sea-level cycle (120 ka to present), all
islands have been larger and better connected than they are
now (Fig. 5). Glacial periods with relatively low sea levels
represent 90% of the last 0.9 Myr (Ruddiman, 2003). During
the last sea-level rise, and within the space of only two millennia, many islands abruptly decreased in surface area by
more than 50%, or became divided into several islands. The
current interglacial Holocene configuration of archipelagos
and island surface areas is the exception, rather than the rule,
with the current island surface area being representative of
only 10% of the last 0.9 Myr. The degree of change in the
surface area of volcanic oceanic islands is a function of both
sea-level fluctuations and island morphometry, where morphometry depends to a large extent on the age or ‘ontogenetic stage’ of an island (cf. Whittaker et al., 2007, 2008).
Older (> 4 Myr) and more eroded islands will change to a
larger degree than younger and steeper islands because of
their generally larger submarine insular shelves (Ramalho
et al., 2013). They show a high surface-area change ratio
(island surface area during glacial maximum divided by its
present surface area, AC > 1.5) during a sea-level cycle, as
seen for Santa Maria (age 8.12 Myr, AC 1.8) in the Azores
and Maio (21 Myr, AC 4.2) in the Cape Verde archipelago.
In contrast, younger islands are affected minimally by sealevel changes because of their steep submarine topography,
as seen for El Hierro (2 Myr, AC 1.3) in the Canaries and
Fogo (2 Myr, AC 1.1) in Cape Verde. Very young islands
(< 1 Myr) in the early stages of emergence, characterized by
low surface area and relatively low elevation, may also be
Table 2 The number of single-island plant endemics (SIEs), multiple-island plant endemics (MIEs) and two-island plant endemics
(2MIEs) of all the nearest island pairs of the Canarian archipelago (EH, El Hierro; LG, La Gomera; LP, La Palma; TF, Tenerife; GC,
Gran Canaria; FV, Fuerteventura; LZ, Lanzarote; MH, Mahan). Coastal, coastal shrub vegetation; Thermo, thermophilous woodland
vegetation. Minimum distance is the present-day distance between island pairs in kilometres (rounded to 0.5 km); Pleistocene distance
is the distance between island pairs during the Last Glacial Maximum (LGM), when sea level was at its lowest. Pleistocene distance was
derived from palaeo-bio-island GIS model (p-BIG model) palaeomaps of 20 ka with mean sea level (MSL) below –120 m.
Island pairs
Minimum
distance
LGM
distances
Vegetation
community
Total sum
of SIEs
Total MIEs
Total 2MIEs
% 2MIEs/SIEs
EH
EH
LP
LP
LG
TF
GC
FV
GC
EH
EH
LP
LP
LG
TF
GC
FV
GC
61.5
67.5
57.5
85.0
27.5
61.0
85.5
11.0
85.5
61.5
67.5
57.5
85.0
27.5
61.0
85.5
11.0
85.5
57.9
66.3
49.5
82.3
20.0
50.6
53.3
0.0
53.3
57.6
66.3
49.5
82.3
20.0
50.6
53.3
0.0
53.3
Coastal
Coastal
Coastal
Coastal
Coastal
Coastal
Coastal
Coastal
Coastal
Thermo
Thermo
Thermo
Thermo
Thermo
Thermo
Thermo
Thermo
Thermo
22
16
22
60
66
77
32
17
55
38
23
39
59
74
84
42
10
57
46
41
48
50
58
53
9
27
9
39
37
44
44
48
43
2
16
2
1
0
0
3
7
10
0
13
1
2
2
0
3
7
7
0
10
1
4.5
0.0
0.0
5.0
10.6
13.0
0.0
76.5
1.8
5.3
8.7
0.0
5.1
9.5
8.3
0.0
100.0
1.8
LG
LP
LG
TF
TF
GC
FV
LZ
MH
LG
LP
LG
TF
TF
GC
FV
LZ
MH
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
7
K. F. Rijsdijk et al.
14
8
12
Number of 2MIEs
10
+
6
8
8
5
6
4
+
2
0
2
1
2
7
3
20
+
3+
+7
1
40
+ 6+
5
+4
9 +9
4
60
Number of SIEs
Figure 5 Relationship between the number of single-island
plant endemics (SIEs) and two-island endemics (2MIEs) for the
closest Canarian island pairs (each symbol representing one pair
of islands) for coastal shrub species (solid dots) and
thermophilous woodland species (+). The solid line (model 6,
2MIE = 0.13 9 SIE – 3) represents islands that were not
connected in the past, and the dotted line (model 6,
2MIE = 0.13 9 SIE + 10) represents islands that were connected
in the past. Numbers coincide with island pairs: 1, El Hierro–La
Gomera; 2, El Hierro–La Palma; 3, La Palma–La Gomera; 4, La
Palma–Tenerife; 5, La Gomera–Tenerife; 6, Tenerife–Gran
Canaria; 7, Gran Canaria–Fuerteventura; 8, Fuerteventura–
Lanzarote; 9, Gran Canaria–Mahan (Fuerteventura–Lanzarote
united).
more sensitive to sea-level fluctuation with high ACs, as is
the case for Corvo (0.7 Myr, AC 2.2) in the Azores.
Biogeographical implications
Surface-area change has biogeographical implications for both
migration and extinction probabilities, as well as speciation
within an island. Present-day species distributions and species
richness have been influenced by a history of changing surface
area, connectivity and isolation driven by sea-level rise
(Fig. 1, point E). This may be reflected by the significantly
high proportion of shared Insecta, Coleoptera and Plantae
2MIEs, on Lanzarote and Fuerteventura, which have, for most
of their history, been a single island, Mahan. This island
existed for more than 110 kyr during the last sea-level cycle,
with the terrestrial fauna and flora being separated three
times for much shorter periods (< 10 kyr) (Fig. 4c). The past
unification of the two contemporary islands must have promoted dispersal, leading to a higher proportion of shared species between the two contemporary islands, compared with
island pairs that have never been connected. We cannot
exclude the possibility that the lower proportion of shared Insecta species between La Gomera and Tenerife is a function
of the greater geographical distance (28 km) between them,
compared with Lanzarote and Fuerteventura (11 km). However, the distance between La Gomera and Tenerife was
reduced by c. 33% to only 20 km during the glacial period,
facilitating inter-island dispersal. The higher percentage of
plant 2MIEs within similar habitats on Lanzarote and Fuerteventura, compared with all other island pairs, points to a
more fundamental biogeographical relationship. This suggests
that the flora of Lanzarote and Fuerteventura is consistent
with expectations for a single island. Given that during the
last 0.9 Myr, sea-level cycles were asymmetric, with longer
periods of lowstands (90% of the time), islands such as Fuerteventura and Lanzarote are, in historical terms, single islands.
Consequently, SIEs that evolved on the palaeo-island Mahan
were separated for only relatively brief periods in interstadials
and interglacial periods, giving rise to 2MIEs. If the situation
was reversed, and the period of island unity during the Pleistocene was much shorter (e.g. 10%) than island separation
(e.g. 90%), allopatric speciation would be expected to have
had greater precedence, and the ratios of 2MIEs to SIEs
would be expected to have been similar to island pairs that
had never been united. Given the asymmetric character of
sea-level cycle periodicities over the last 1 Myr, we predict
that this pattern of shared MIEs and shared species of
Table 3 Modelled surface-area change of Macaronesian archipelago volcanic islands driven by mean sea level (MSL) fluctuations
ordered according to increasing corrected Akaike information criterion (AICc) values, showing that models 7 and 6, with single-island
endemics (SIEs) + past connectedness + distance, are consistent with the data. The residuals for the fitted models 6 and 7 do not
deviate from a Gaussian distribution. MIEs, multiple-island endemics; comb, a categorical variable indicating whether an island pair was
connected in the past or not. See Appendix S.3 for the annotated R script with data and results.
Models
AICc
DAICc
AICcWt
Significant model
R2adj
P
7
6
4
1
5
3
1
70.35
70.87
84.30
86.37
88.45
89.48
98.10
0.00
0.52
13.95
16.02
18.10
19.13
27.75
0.56
0.44
0.00
0.00
0.00
0.00
0.00
2MIEs = 0.63 – 0.05D + 0.12 SIEs + 9.8comb
2MIEs = –3.0 + 0.13 SIEs + 12.8comb
–
–
–
–
–
0.78
0.84
–
–
–
–
–
< 0.001
< 0.001
–
–
–
–
–
DSIEcomb
SIEcomb
DSIE
D
Dcomb
comb
SIE
DAICc, Akaike difference: the difference of a model’s AICc value and the lowest AICc value in the set of models. AICcWt, Akaike weight: the
probability that a given model is the best model from the set. R2adj, adjusted R2: the proportion of the total sum of squares explained by the
model adjusted for the number of predictor variables in the model.
8
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
formerly merged islands is likely to be a global pattern for
islands that were connected during glacial periods (e.g.
Moody, 2000; Price & Elliott-Fisk, 2004). Although LGM distances to continents were not selected as significant predictors, we expect that they may be a significant predictor in
settings characterized by higher surface-area changes (e.g.
Cape Verde). Although statistically valid, our assessments are
limited to a single archipelago and comprise a heterogeneous
set of data. Further testing of our hypothesis with data from
other pairs of previously united islands will be essential to
assess its general validity (e.g. Ali & Aitchison, 2014).
It could be postulated that a higher degree of habitat and
climatological similarity between the formerly united islands
of Lanzarote and Fuerteventura may explain a higher proportion of shared species between this island pair. However, habitats and climatic conditions of Lanzarote and Fuerteventura
are not necessarily more similar when compared with other
island pairs (Carracedo, 2008, 2009; Hooghiemstra et al.,
2014). During glacial periods, the similar habitats of Fuerteventura and Lanzarote were connected, and thus larger in
size, and this may have promoted higher rates of in situ speciation, as predicted by the species pool hypothesis (Taylor et al.,
1990; Zobel et al., 2011). Indeed, Zobel et al. (2011) have
shown that both native non-endemic richness and SIE richness
(in situ speciation) within the same habitat increase with habitat size and habitat age on the Canary Islands. A quantitative
assessment that includes a habitat diversity assessment per
island would provide a more definitive answer.
Geological complexity
Geological events also may play an important role by directly
affecting island areas and connectivity. Examples include volcanism by progradation of coastal lava deltas, and coastal
erosion by wave action or mass wasting (Ramalho et al.,
2013). While a global MSL curve is used to quantify changes
in island surface area, several factors might lead to local deviations. As a result of various geological factors, volcanic oceanic islands may sink or rise (e.g. Price & Elliott-Fisk, 2004;
Menendez et al., 2008; Whittaker et al., 2008; Ramalho et al.,
2010; Ali & Aitchison, 2014). In the Canary Islands, raised
Pliocene sea-level markers such as pillow lavas indicate maximum mean uplift rates of between 0.022 and 0.024 m kyr 1
(Meco et al., 2002; Zazo et al., 2003, 2007; Menendez et al.,
2008). These local uplift rates do not significantly modify the
eustatic sea-level rise curves for the last 120 kyr. Another factor that may lead to regional deviations from the global sea
level curve is the global redistribution of melt-water in the
oceans, leading to ocean water loading effects of the lithosphere and differential crustal flexing (Lambeck & Chappell,
2001; Gehrels & Long, 2008; Milne & Mitrovica, 2008; Ali &
Aitchison, 2014). However, effects that have been recorded
within the tropical and subtropical near-coastal zone are generally in the order of several metres during the last maximum sea-level rise of 120 m, suggesting that the total
contribution of this component is minor. A final potential
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
effect is that melt-water is not evenly distributed across the
globe as a result of the dynamic interplay between the gravitational pull of ice sheets and the ocean water mass. For the
Azores, this effect amounts to c. 10 m (Milne & Mitrovica,
2008). Although the individual effects of local factors modifying change in island surface area may be limited during
one sea-level cycle (120 kyr), their combined effects may
complicate sea-level based reconstructions of palaeo-islands.
Speciation and extinction rates
Our models raise the question of how asymmetric cyclical
separation and unification of islands such as Fuerteventura
and Lanzarote may have affected both allopatric speciation
and (local/global) extinction rates. Changes in inter-insular
and island–mainland distances and, in extreme cases, the
unification or splitting of islands (e.g. Faial with Pico;
Madeira with Desertas; Lanzarote with Fuerteventura and
related islets; S~ao Vicente, Santa Lucia, Branco and Raso;
Figs 4 & 5) will alter colonization probabilities. Species, or
differentiated populations within species, on islands that
became reconnected during sea-level falls after being isolated
may have experienced interspecific competition or hybridization, or evolutionary responses that facilitated coexistence
(e.g. Emerson & Kolm, 2005). In addition, periodic island
surface-area increases may have promoted adaptive radiation
and diversification (Price & Elliott-Fisk, 2004; Gavrilets &
Vose, 2005; Kisel & Barraclough, 2010; Papadopulos et al.,
2011). As a consequence of the predictions of the dynamic
equilibrium model of island biogeography (MacArthur &
Wilson, 1967), surface-area reductions as a result of sea-level
rise should lead to area-dependent extinctions or so called
‘relaxation’ events (Diamond, 1972; Wilcox, 1978; Richman
et al., 1988; Mayr & Diamond, 2001; Louys et al., 2007). In
continental island settings, sea level-related natural Pleistocene extinctions are attributed to one of two mechanisms.
The first is alien continental species invading the islands
through filter bridges or sweepstake dispersal during glacial
marine lowstands (e.g. Sondaar & Van der Geer, 2005). The
second mechanism is surface-area reduction resulting from
interglacial sea-level rise (e.g. Heaney, 1984; Gardner, 1986;
McFarlane et al., 1998; Foufopoulos & Ives, 1999; Davalos &
Russell, 2012). Oceanic volcanic islands with high endemism
and an absence of confounding continental land-bridge
interactions are ideal settings for assessing the role of changing sea levels. Intriguingly, in spite of extensive palaeontological and archaeological surveys, particularly for the recent
period of sea-level rise (16 ka to present), virtually no empirical (fossil) evidence exists for natural global extinctions on
oceanic volcanic islands (e.g. Steadman, 2006; Rando et al.,
2008; Turvey, 2009; Simberloff & Collins, 2010; Illera et al.,
2012). Clearly, low sea levels persist long enough during sealevel cycles (90%) for species to accumulate; however, with a
lack of evidence for extinction, it may be that the relaxation
time for species is longer than the relatively short intervals
during which islands became geographically independent or
9
K. F. Rijsdijk et al.
decreased in size (10% of the time) (Losos, 1986). Non-volant
insular biota, being locked on oceanic islands, were forced to
endure the combined effects of climate and sea-level changes,
and this may have contributed to an increase in their resil
ience (Emerson & Kolm, 2005; Avila
et al., 2008; Rijsdijk
et al., 2011; de Boer et al., 2013, 2014; Hooghiemstra et al.,
2014). Anthropogenic change has led to massive species
extinctions on volcanic islands, which are currently at their
long-term minimum surface area and most isolated configurations. This suggests that remaining insular biotas may be
particularly vulnerable to increasing human impact and further sea-level rise (Wetzel et al., 2012; Bellard et al., 2014).
CONCLUSIONS
Contemporary island area and related features, such as shape,
elevation, isolation and geographical configuration of archipelagos, represent transitory stages that are the result of two
long-term dynamic processes: (1) the ontogenetic history of
the volcanic islands themselves, lasting millions of years
(Whittaker et al., 2007, 2008), and (2) the Pleistocene sealevel cycles, lasting many millennia (Warren et al., 2010;
Fernandez-Palacios et al., 2011; Avila,
in press). Therefore it
is important that a general dynamic theory (Brown & Lomolino, 2000; Heaney, 2000, 2007; Whittaker et al., 2008) should
take both these processes into account for a meaningful interpretation of the biogeographical, ecological and evolutionary
processes shaping present-day insular biotic assemblages, as
well as the geographical distributions of constituent species.
ACKNOWLEDGEMENTS
We acknowledge valuable discussions with Robert Whittaker,
Kostas Triantis, Ben Warren, James Rosindell, Henry Hooghiemstra, Erik de Boer, Jens Zinke and Christophe Thebaud.
We thank Lawrence Heaney, Kostas Triantis, Sean Connolly
and two anonymous referees for their feedback. We thank
DodoAlive for the funding of an ad hoc sea level workshop
held in 2010 at the University of Oxford, a Ci^encia 2008
research contract funded by Fundacß~ao para a Ci^encia e a
Tecnologia (FCT), and the organizers of the workshop ‘Climate change perspectives from the Atlantic: past, present and
future’ held at La Laguna University, Tenerife, in October
2012 for providing a stage for presenting and discussing
some of the results presented in this paper. We also acknowledge feedback on our poster presentations at the fifth and
sixth biannual symposia of the International Biogeographical
Society (IBS) in Crete, Greece, in 2011, and in Miami, Florida, USA, in 2013. We thank the CESAB Islands initiative
(http://www.cesab.org/) for creating a platform that includes
further research on this topic.
REFERENCES
Ali, J.R. & Aitchison, J.C. (2014) Exploring the combined
role of eustasy and oceanic island thermal subsidence in
10
shaping biodiversity on the Galapagos. Journal of Biogeography, doi:10.1111/jbi.12313.
Arechavaleta, M., Rodrıguez, S., Zurita, N. & Garcıa, A.
(2010) Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres, 2009. Gobierno de Canarias, Santa
Cruz de Tenerife, Tenerife.
Avila,
S.P. (2000) Shallow-water marine molluscs of the Azores: biogeographical relationships. Arquipelago, Life and
Marine Sciences, Supplement 2 (Part A), 99–131.
Avila,
S.P. (2014) Unravelling the patterns and processes of
evolution of marine life in oceanic islands: a global framework. Climate change perspectives from the Atlantic: past,
present and future (ed. by J.M. Fernandez-Palacios, L. de
Nascimento, J.C. Hernandez, S. Clemente, A. Gonzalez
and J.P. Dıaz-Gonzalez). La Laguna University Press, La
Laguna, Tenerife. pp. 95–125.
Avila,
S.P. & Malaquias, M.A.E. (2003) Biogeographical relationships of the molluscan fauna of the Ormonde seamount (Gorringe bank, northeast Atlantic Ocean).
Journal of Molluscan Studies, 69, 145–150.
Avila,
S.P., Melo, P.J., Lima, A., Martins, A.M.F. & Rodrigues, A. (2008) The reproductive cycle of the rissoid Alvania mediolittoralis Gofas, 1989 (Mollusca, Gastropoda) at
S~ao Miguel Island (Azores, Portugal). Invertebrate Reproduction and Development, 52, 31–40.
Avila,
S.P., Silva, C.M., Sciebel, R., Cecca, F., Backeljau, T. &
Martins, A.M.F. (2009) How did they get here? Palaeobiogeography of the Pleistocene marine molluscs of the Azores.
Bulletin of the Geological Society of France, 180, 295–307.
Becker, J.J., Sandwell, D.T., Smith, W.H.F., Braud, J., Binder,
B., Depner, J., Fabre, D., Factor, J., Ingalls, S., Kim, S.-H.,
Ladner, R., Marks, K., Nelson, S., Pharaoh, A., Trimmer,
R., Von Rosenberg, J., Wallace, G. & Weatherall, P. (2009)
Global bathymetry and elevation data at 30 arc seconds
resolution: SRTM30_PLUS. Marine Geodesy, 32, 355–371.
Bellard, C., Leclerc, C. & Courchamp, F. (2014) Impact of
sea level rise on the 10 insular biodiversity hotspots. Global Ecology and Biogeography, 23, 203–212.
Bintanja, R., van de Wal, R.S.W. & Oerlemans, J. (2005)
Modelled atmospheric temperatures and global sea levels
over the past million years. Nature, 437, 125–128.
Bivand, R., Pebesma, E. & Rubio, V. (2008) Applied spatial
data analysis with R. Springer, Heidelberg.
de Boer, E.J., Hooghiemstra, H., Vincent Florens, F.B., Baider, C., Engels, S., Dakos, V., Blaauw, M. & Bennett, K.D.
(2013) Rapid succession of plant associations on the small
ocean island of Mauritius at the onset of the Holocene.
Quaternary Science Reviews, 68, 114–125.
de Boer, E.J., Tjallingii, R., Velez, M.I., Rijsdijk, K.F., Vlug,
A., Reichart, G.-J., Prendergast, A.L., de Louw, P.G.B.,
Vincent Florens, F.B., Baider, C. & Hooghiemstra, H.
(2014) Climate variability in the SW Indian Ocean from a
8000-yr long multi-proxy record in the Mauritian lowlands shows a middle to late Holocene shift from negative
IOD-state to ENSO-state. Quaternary Science Reviews, 86,
175–189.
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
Brown, J.H. & Lomolino, M.V. (2000) Concluding remarks:
historical perspective and the future of island biogeography theory. Global Ecology and Biogeography, 9, 87–92.
Burnham, K.P. & Anderson, D.R. (2002) Model selection and
multimodel inference, a practical information-theoretic
approach, 2nd edn. Springer-Verlag, New York.
Camoin, G., Montaggioni, L. & Braithwaite, C. (2004) Late
glacial to post glacial sea levels in the Western Indian
Ocean. Marine Geology, 206, 119–146.
Carracedo, J.C. (2008) Los volcanes de las Islas Canarias –
Canarian volcanoes. IV. La Palma, La Gomera y El Hierro.
Editorial Rueda SL, Madrid.
Carracedo, J.C. (2009) Geologıa de Canarias I (Origen, evolucion, edad y volcanismo). Editorial Rueda SL, Madrid.
Cutler, K.B., Edwards, R.L., Taylor, F.W., Cheng, H., Adkins,
J., Gallup, C.D., Cutler, P.M., Burr, G.S. & Bloom, A.L.
(2003) Rapid sea-level fall and deep-ocean temperature
change since the last interglacial period. Earth and Planetary Science Letters, 206, 253–271.
Davalos, L.M. & Russell, A.L. (2012) Deglaciation explains
bat extinction in the Caribbean. Ecology and Evolution, 2,
3045–3051.
Diamond, J. (1972) Biogeographical kinetics: estimation of
relaxation times for avifaunas of southwest Pacific islands.
Proceedings of the National Academic of Science USA, 69,
3199–3203.
Emerson, B.C. & Kolm, N. (2005) Species diversity can drive
speciation. Nature, 434, 1015–1017.
Fernandez-Palacios, J.M., de Nascimento, L., Otto, R., Delgado, J.D., Garcıa-del-Rey, E., Arevalo, J.R. & Whittaker,
R.J. (2011) A reconstruction of Palaeo-Macaronesia, with
particular reference to the long-term biogeography of the
Atlantic island laurel forests. Journal of Biogeography, 38,
226–246.
Foufopoulos, J. & Ives, A.R. (1999) Reptile extinctions on
land-bridge islands: life-history attributes and vulnerability
to extinction. The American Naturalist, 153, 1–25.
Garcıa-Talavera, F. (1999) Consideraciones geol
ogicas, biogeograficas y paleoecol
ogicas. Ecologıa y cultura en Canarias
(ed. by J.M. Fernandez-Palacios, J.J. Bacallado and J.A. Belmonte), pp. 39–63. Museo de la Ciencia y el Cosmos, Cabildo Insular de Tenerife, Santa Cruz de Tenerife, Tenerife.
Gardner, A.S. (1986) The biogeography of the lizards of the
Seychelles Islands. Journal of Biogeography, 13, 237–253.
Gavrilets, S. & Vose, A. (2005) Dynamic patterns of adaptive
radiation. Proceedings of the National Academy of Sciences
USA, 102, 18040–18045.
Gehrels, R. & Long, A. (2008) Sea level is not level. Geography, 93, 11–16.
Gofas, S. (2007) Rissoidae (Mollusca: Gastropoda) from
northeast Atlantic seamounts. Journal of Natural History,
41, 779–885.
Heaney, L.R. (1984) Mammalian species richness on islands
on the Sunda Shelf, Southeast Asia. Oecologia, 61, 11–17.
Heaney, L.R. (1986) Biogeography of mammals in SE Asia:
estimates of rates of colonization, extinction and
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
speciation. Biological Journal of the Linnean Society, 28,
127–165.
Heaney, L.R. (2000) Dynamic disequilibrium: a long-term,
large-scale perspective on the equilibrium model of island
biogeography. Global Ecology and Biogeography, 9, 59–74.
Heaney, L.R. (2007) Is a new paradigm emerging for oceanic
island biogeography? Journal of Biogeography, 34, 753–757.
Hengl, T. (2009) A practical guide to geostatistical mapping.
University of Amsterdam, Amsterdam.
Hijmans, R., Garcia, N. & Wieczorek, J. (2010) GADM: database of global administrative areas. Version 1. Available at:
http://www.gadm.org/ (accessed 17 February 2010).
Hooghiemstra, H., Rijsdijk, K.F., de Boer, E., Florens, V. &
Baider, C. (2014) Insular environmental change; climateforced and system-driven. Climate change perspectives from
the Atlantic: past, present and future (ed. by J.M. Fernandez-Palacios, L. de Nascimento, J.C. Hernandez, S. Clemente, A. Gonzalez and J.P. Dıaz-Gonzalez). La Laguna
University Press, La Laguna, Tenerife. pp. 51–74.
Illera, J.C., Rando, J.C., Richardson, D.S. & Emerson, B.C.
(2012) Age, origins and extinctions of the avifauna of
Macaronesia: a synthesis of phylogenetic and fossil information. Quaternary Science Reviews, 50, 14–22.
Kisel, Y. & Barraclough, T.G. (2010) Speciation has a spatial
scale that depends on levels of gene flow. The American
Naturalist, 175, 316–334.
Lambeck, K. & Chappell, J. (2001) Sea level change through
the last glacial cycle. Science, 312, 679–686.
Lambeck, K., Esat, T.M. & Potter, E.-K. (2002) Links
between climate and sea levels for the past three million
years. Nature, 419, 199–206.
Losos, J.B. (1986) Island biogeography of day geckos (Phelsuma) in the Indian Ocean. Oecologia, 68, 338–343.
Louys, J., Curnoe, D. & Tong, H. (2007) Characteristics of
Pleistocene megafauna extinctions in Southeast Asia. Palaeogeography, Palaeoclimatology, Palaeoecology, 243, 152–
173.
MacArthur, R.H. & Wilson, E.O. (1967) The theory of island
biogeography. Princeton University Press, Princeton, NJ.
Mayr, E. (1944) Wallace’s line in the light of recent zoogeographic studies. Quaternary Review of Biology, 19, 1–14.
Mayr, E. & Diamond, J. (2001) The birds of northern Melanesia: speciation, ecology, and biogeography. Oxford University, Oxford.
McFarlane, D.A., MacPhee, R.D.E. & Ford, D.C. (1998) Body
size variability and a Sangamonian extinction model for
Amblyrhiza a West Indian megafaunal rodent. Quaternary
Research, 50, 80–89.
Meco, J., Guillou, H., Carracedo, J.-C., Lomoschitz, A., Ramos, A.-J.G. & Rodrıguez-Yanez, J.-J. (2002) The maximum warmings of the Pleistocene world climate recorded
in the Canary Islands. Palaeogeography, Palaeoclimatology,
Palaeoecology, 185, 197–210.
Menendez, I., Silva, P.G., Martın-Betancor, M., Perez-Torrado, F.J., Guillou, H. & Scaillet, S. (2008) Fluvial dissection,
isostatic uplift, and geomorphological evolution of
11
K. F. Rijsdijk et al.
volcanic islands (Gran Canaria, Canary Islands, Spain).
Geomorphology, 102, 189–203.
Milne, G.A. & Mitrovica, J.X. (2008) Searching for eustasy in
deglacial sea-level histories. Quaternary Science Reviews, 27,
2312–2302.
Moody, A. (2000) Analysis of plant species diversity with
respect to island characteristics on the Channel Islands,
California. Journal of Biogeography, 27, 711–723.
Papadopulos, A.S.T., Baker, W.J., Crayn, D., Butlin, R.K.,
Kynast, R.G., Hutton, I. & Savolainen, V. (2011) Speciation with gene flow on Lord Howe Island. Proceedings of
the National Academy of Sciences USA, 108, 13188–13193.
Patterson, T.C. (2007) Google Earth as a (not just) geography education tool. Journal of Geography, 106, 145–152.
Peltier, W.R. & Fairbanks, R.G. (2006) Global glacial ice volume and Last Glacial Maximum duration from an
extended Barbados sea level record. Quaternary Science
Reviews, 25, 3322–3337.
Price, J.P. & Elliott-Fisk, D. (2004) Topographic history of
the Maui Nui complex, Hawai’i, and its implications for
biogeography. Pacific Science, 58, 27–45.
Qian, H. & Ricklefs, R.E. (2000) Large-scale processes and
the Asian bias in species biodiversity of temperate plants.
Nature, 407, 180–182.
R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing,
Vienna, Austria.
Ramalho, R., Helffrich, G., Cosca, M., Vance, D., Hoffmann,
D. & Schmidt, D.N. (2010) Episodic swell growth inferred
from variable uplift of the Cape Verde hot spot islands.
Nature Geoscience, 3, 774–777.
Ramalho, R.S., Quartau, R., Trenhaile, A.S., Mitchell, N.C.,
Woodroffe, C.D. & Avila,
S.P. (2013) Coastal evolution in
oceanic islands: a complex interplay between volcanism,
erosion, sedimentation and biogenic production. Earth Science Reviews, 127, 140–170.
Rando, J.C., Alcover, J.A., Navarro, J.F., Garcıa-Talavera, F.,
Hutterer, R. & Michaux, J. (2008) Chronology and causes
of the extinction of the Lava Mouse, Malpaisomys insularis
(Rodentia: Muridae) from the Canary Islands. Quaternary
Research, 70, 141–148.
Richman, A.D., Case, T.J. & Schwaner, T.D. (1988) Natural
and unnatural extinction rates of reptiles on islands. The
American Naturalist, 131, 611–630.
Rijsdijk, K.F., Zinke, J., de Louw, P.G.B., Hume, J.P., van der
Plicht, H., Hooghiemstra, H., Meijer, H.J.M., Vonhof,
H.B., Porch, N., Florens, F.B.V., Baider, C., van Geel, B.,
Brinkkemper, J., Vernimmen, T. & Janoo, A. (2011) MidHolocene (4200 kyr bp) mass mortalities in Mauritius
(Mascarenes): insular vertebrates resilient to climatic
extremes but vulnerable to human impact. The Holocene,
21, 1179–1194.
Ruddiman, W.F. (2003) Orbital insolation, ice volume, and
greenhouse gases. Quaternary Science Reviews, 22, 1597–1631.
Simberloff, D. & Collins, M.D. (2010) The domain of the
dynamic equilibrium theory and assembly rules with com12
ments on the taxon cycle. The theory of island biogeography
revisited (ed. by J.B. Losos and R.E. Ricklefs), pp. 237–263.
Princeton University Press, Princeton, NJ.
Sondaar, P.Y. & Van der Geer, A.A.E. (2005) Evolution and
extinction of Plio-Pleistocene island ungulates. Les ongules
holarctiques du Pliocene et du Pleistocene (ed. by E. CregutBonnoure), pp. 241–256. Quaternaire, International Journal of the French Quaternary Association, hors-serie 2.
Maison de la Geologie, Paris.
Steadman, D.W. (2006) Extinction and biogeography of tropical Pacific birds. University of Chicago Press, Chicago.
Taylor, D.R., Aarssen, L.W. & Loehle, C. (1990) On the relationship between r/K selection and environmental carrying
capacity: a new habitat template for plant life history strategies. Oikos, 58, 239–250.
Turvey, S.T. (ed.) (2009) Holocene extinctions. Oxford University Press, Oxford.
Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations.
Journal of Biogeography, 27, 1153–1167.
Warren, B.H., Strasberg, D., Bruggemann, J.H., Prys-Jones,
R.P. & Thebaud, C. (2010) Why does the biota of the
Madagascar region have such a strong Asiatic flavor? Cladistics, 26, 526–538.
Wessel, P. & Smith, W.H.F. (1996) A global self-consistent,
hierarchical, high-resolution shoreline database. Journal of
Geophysical Research, 101, 8741–8743.
Wetzel, F.T., Kissling, W.D., Beissmann, H. & Penn, D.J.
(2012) Future climate change driven sea-level rise: secondary consequences from human displacement for island
biodiversity. Global Change Biology, 18, 2707–2719.
Whittaker, R.J., Ladle, R.J., Ara
ujo, M.B., Fernandez-Palacios,
J.M., Delgado, J.D. & Arevalo, J.R. (2007) The island
immaturity speciation pulse model of island evolution: an
alternative to the ‘diversity begets diversity’ model. Ecography, 30, 321–327.
Whittaker, R.J., Triantis, K. & Ladle, R.J. (2008) A general
dynamic theory of oceanic island biogeography. Journal of
Biogeography, 35, 977–994.
Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2010) A general
dynamic theory of oceanic island biogeography: extending
the MacArthur–Wilson theory to accommodate the rise
and fall of volcanic islands. The theory of island biogeography revisited (ed. by J.B. Losos and R.E. Ricklefs), pp. 88–
115. Princeton University Press, Princeton, NJ.
Wilcox, B.A. (1978) Supersaturated island faunas: a species–
age relationship for lizards on post-Pleistocene land-bridge
islands. Science, 199, 996–998.
Zazo, C., Goy, J.L., Dabrio, C.J., Bardajı, T., Hillaire-Marcel,
& Soler, V. (2003)
C., Ghaleb, B., Gonzalez-Delgado, J.-A.
Pleistocene raised marine terraces of the Spanish Mediterranean and Atlantic coasts: records of coastal uplift, sealevel highstands and climate changes. Marine Geology, 194,
103–133.
Zazo, C., Goy, J.L., Dabrio, C.J., Soler, V., Hillaire-Marcel,
C., Ghaleb, B., Gonzalez-Delgado, J.A., Bardajı, T. &
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
Biogeographical implications of Pleistocene sea-level change
Cabero, A. (2007) Quaternary marine terraces on Sal
Island (Cape Verde archipelago). Quaternary Science
Reviews, 26, 876–893.
Zinke, J., Reijmer, J.J.G., Thomassin, B.A. & Dullo, W.
(2001) Postglacial flooding history of Mayotte Lagoon
(Comoro Archipelago, southwest Indian Ocean). Marine
Geology, 194, 181–196.
Zobel, M., Otto, R., Laanisto, L., Naranjo-Cigala, A., P€artel,
M. & Fernandez-Palacios, J.M. (2011) The formation of
species pools: historical habitat abundance affects local
diversity. Global Ecology and Biogeography, 20, 251–259.
BIOSKETCH
This paper has been written by an interdisciplinary ad hoc
group sharing a fascination for island biogeography.
Author contributions: K.F.R. initiated and coordinated the
research; T.H. programmed p-BIG in R; S.N. improved
p-BIG and analysed the results; J.M.F.-P. and B.E. substantially contributed to the theory and writing; E.v.L. led the
statistical analyses; other authors provided data, performed
analyses and contributed essential insights; K.F.R., J.M.F.P.
and B.C.E. led the writing.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the
online version of this article:
Editor: Lawrence Heaney
Appendix S1 Surface areas and distance to continents.
Appendix S2 Annotated R scripts.
Appendix S3 Shared species filtering.
Journal of Biogeography
ª 2014 John Wiley & Sons Ltd
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