www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 939
Geology, climate, size, the degree of isolation, the distance
from the mainland, vegetation cover, and local fauna
all add to the complexity of island environments. Islands
are natural laboratories for observing how ecological and
evolutionary processes shape isolated communities. Islands
and their communities gradually change over long periods
of time; at any given point, they are the result of intricate,
interdependent combinations of geological, climatologi-
cal, and biological factors. It would follow that their study
is an ideal case for collaboration among different kinds of
specialists. Hypotheses and models developed jointly by bio-
logists, zoologists, ecoethologists, geneticists, and paleontol-
ogists could beneﬁt from this collaboration. Unfortunately,
however, this sort of cooperation rarely occurs.
There are many examples of open or unresolved issues in
the ﬁeld. For example, controversy among bio geographers
(Grande 1990) revolves around whether insular faunas
derive from dispersal or from vicariance (i.e., the geographi-
cal separation and isolation of a subpopulation), but these
two processes can be part of the same chronological event
(Masini et al. 2002). Under the effects of sea-level changes
or tectonic movements, a land bridge that originally func-
tioned as a freely accessible, two-way connection may
gradually morph into an ever-more-ﬁltering corridor and
may eventually sink, leaving an island—and its fauna—in
complete isolation. The understanding of such a complex
process can be reached only by taking a multidisciplinary
perspective that encompasses not only biogeographic fac-
tors but also geological processes, climatic inﬂuences, and
In numerous studies, starting with Darwin’s (1859) and
Wallace’s (1869) historical treatises and continuing into
the twentieth century (e.g., Simpson 1940, McKenna 1973),
contrasting modes of island colonization have been sug-
gested (table 1). Some of the more recent researchers (e.g.,
Dermitzakis and Sondaar 1978, van den Hoek Ostende et al.
2009, variously inspired by Matthew 1939) have considered
sweepstake migration—the sporadic, accidental, and highly
selective dispersal from a continent to an island by way of
swimming or natural rafting—as the most likely and most
common process of colonization. According to some scien-
tists (e.g., van den Hoek Ostende et al. 2009), a two-way con-
nection with the mainland would produce balanced insular
fauna or fossil assemblages (a balanced fauna is in a state of
equilibrium). Sweepstake colonization (in which not all the
ecological niches that occur on the mainland are actually
occupied) would instead result in unbalanced insular mam-
mal fauna or fossil assemblages. In the use of these concepts,
it is assumed that the composition of either living or fossil
insular mammalian communities reveals their mechanisms
A Multidisciplinary Approach to
the Analysis of Multifactorial Land
Mammal Colonization of Islands
Paul P. a. Mazza, Sandro lovari, Federico MaSini, Marco MaSSeti, and Marco ruStioni
A highly debated question that engages paleontologists, zoogeographers, and zoologists is how terrestrial mammals colonize islands. The question’s
oversimpliﬁcation and the subjective and partial responses to it have led to reductionist models. Insular faunas and fossil assemblages result from
a complex interaction of geological, biological (in a broad sense), climatic, eustatic, taphonomic, and historical processes. Insular assemblages
and their accompanying variables should be investigated on a case-by-case basis. In this article, we discuss not only common misconceptions and
their potential origins but also the key issues that should be addressed when dealing with the colonization of islands by land mammals. We call
for the implementation of multi- and interdisciplinary research programs and teamwork, involving paleontological, geological, and stratigraphic
information; climatological factors; sea-level evolution; sampling and analytical biases; ecological, physiological, taphonomic, and environmental
factors; behavioral characters and ecological preferences; genetics; phylogeography; densities of colonizing populations; and historical reports of
human-mediated faunal introductions.
Keywords: dispersal, insular immigration, therians, modeling, vicariance
BioScience 63: 939–951. ISSN 0006-3568, electronic ISSN 1525-3244. © 2013 by American Institute of Biological Sciences. All rights reserved. Request
permission to photocopy or reproduce article content at the University of California Press’s Rights and Permissions Web site at www.ucpressjournals.com/
940 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
of dispersal to islands (see Palombo 2009a and the references
We contend that this is an oversimpliﬁcation. Insular ter-
restrial mammal communities, either living or fossil, can
be found to be unbalanced for many more reasons than a
sweepstake invasion by new species. For example, faunal
relaxation (i.e., the loss of species from newly isolated
islands under environmental or other pressures resulting
from the island environment itself, as in Brown JH 1971)
and selective preservation (in which species exhibit different
preservation potential, depending on the durability of their
skeletons) need to be considered in unbalanced assemblages:
Ecological, taphonomic, and stratigraphic issues therefore
need to be taken into account simultaneously. Just why
insular mammal communities are unbalanced is a key issue
for debate in the ﬁeld, as we shall see.
Increasingly, multiproxy and interdisciplinary investiga-
tions are a feature of scientiﬁc research. Here, we emphasize
that solid inferences in the ﬁeld of insular mammal coloniza-
tion can be achieved only through cross-referencing different
but mutually supportive records. We maintain that research
programs in this ﬁeld need to include the examination
of paleontological evidence, together with geological and
stratigraphic information; climate and sea-level evidence;
taphonomic sampling; ecology; the behavioral, genetic, and
physiological characteristics of the colonizing populations;
phylogeography; species densities; and historical records
of human-mediated faunal introductions. Not one of these
areas, in principle, stands above the others in the search for
scientiﬁc truth or models.
Figure 1 is a ﬂow diagram that illustrates this principle
through the key areas of information that need to be con-
sidered in the study of insular land mammals. The graph
also shows the interrelations among and across the different
groups of variables and the many lines of evidence.
Geological, paleontological, and stratigraphic
Many islands (e.g., the Aegean archipelago, the Indonesian
islands) are located in active tectonic belts and are possibly
subject to intense deformation. Consequently, accurately
interpreting geological data (the most comprehensive avail-
able and developed at the ﬁnest resolution level) is crucial
in establishing the relative likelihood of various coloniza-
tion hypotheses, especially because many of these hypo-
theses conform to a biogeographic methodology, which is
dependent on geology. The fossil record, however, is the
primary evidence of faunal dispersal to islands; it indi-
cates how and from where islands were colonized and the
periods during which they were isolated or connected.
Because isolated faunas grow progressively more endemic
as the time of isolation increases, fossils can indicate the
existence of a fossil island—a past colony of mammals on
a once-isolated landmass; they can provide details of the
island’s changes over time. Paleontological data can furnish
useful evidence to help geologists in the reconstruction of
the dynamics of landmasses and of changes in sea level. An
interdisciplinary approach beneﬁts all sides in this research:
Theories can be tested against reconstructions obtained
using the information of other disciplines. For example, the
fossil record provides useful corroboration for geologists in
their reconstructions of the dynamics of landmasses and of
sea-level variation. It also helps paleoclimatologists in their
understanding of how climatic conditions have changed
over time. Conversely, geological and climatic events help
paleontologists deconstruct colonization processes. In addi-
tion, neontologists may use the paleontological record in a
comparative way to reconstruct and understand the coloni-
zation histories of modern insular communities.
Geological and paleontological events are registered in
the terrestrial and marine stratigraphic successions of an
island (ﬁgure 1). The accurate assessment of stratigraphic
and depositional resolutions or the composition of layered
successions is essential not only to estimate the age of colo-
nization events but also to evaluate the strength of geological
and paleontological information. Because of the predomi-
nantly destructive (erosional) conditions on land, terrestrial
stratigraphic successions are usually highly disrupted tem-
poral records from insigniﬁcant spatial areas (McKinney
et al. 1996, Kidwell and Holland 2002). The resolution of
stratigraphic sequences may, however, yield key information
on the sequence and nature of geological events, as well as
on the relative abundance of different components or spe-
cies within a fossil community. Discontinuous stratigraphic
records—or even exceedingly long stratigraphic records—
may register signiﬁcant short-term events, whereas long
records can have the effect of averaging out many short-
term variations. Some species—those with less uniform
distribution in the fossil record—may appear to be more
rare than those that are more evenly distributed (McKinney
et al. 1996). Other difﬁculties can arise from a fossil-bearing
stratum with reworked (exotic) particles and fossils or when
sedimentary structures and diagenetic overprints (post-
burial modiﬁcations) postdate its deposition, thus making
its analysis more difﬁcult. These factors can all strongly bias
the paleontological and paleoecological inferences on past
Table 1. Ways of dispersal and expected characters of
Ways of species dispersal
Characteristics of the resulting
Corridors (pathways devoid of
any physical or ecological barrier)
Balanced (i.e., the community is
sufﬁciently varied to be ecologically
stable) nonendemic fauna
Filter bridges (routes open only
for some species)
Balanced faunas but impoverished
Pendel routes (narrow sea straits
that can be easily crossed by
Unbalanced faunas, with both
endemic and mainland taxa
Sweepstake routes (routes
of sporadic, accidental, and
highly selective dispersal from
continent to island)
Very endemic and unbalanced
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 941
insular life, as well as our reconstructions of past paleogeo-
graphical events and structures.
Marine stratigraphic successions, however, tend to be
much more complete and continuous than terrestrial ones
are. They can only be accessed if they have been exposed
by tectonic disruptions and uplifts or by sea-level drops or
by directly drilling into the sea bottom. Raup (1976) also
showed that the probability of preservation per unit of
geological time is strongly connected with the volume of
local rocky outcrop: Our detailed knowledge of any fossil
record correlates strongly with the amount of rock avail-
able for sampling for the period. The marine sedimentary
and analytical biases
with control of the
and of the
Sea level change through time
Ecological, physiological, and
and ecological preferences
Genetics and densities of colonizing
Information on insular communities
Inferences on insular colonization
overall information permits
possibly contribute to
Figure 1. Data involved in the analysis of insular terrestrial mammalian communities and of their insular colonizations.
The diagram shows the inﬂuence and control exercised by speciﬁc factors on the different records and the interconnections
and data ﬂows between the different ﬁelds of research. Theoretical models of insular colonization should be based on
inferences drawn from two sets of data: (1) the evidence needed to reconstruct an island’s history and (2) information on
past or present insular terrestrial mammal communities.
942 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
deposits around islands are treasure chests of informa-
tion. They can reveal possible moments of surfacing of the
seaﬂoor and, therefore, possible past land-bridge connec-
tions. Exploring them, however, requires expensive offshore
coring. Consequently, many tentative theories on the land
mammal colonization of islands shall remain mere working
hypotheses until that information is revealed. The literature
offers emblematic examples. Crete and Madagascar are
often considered to have been isolated for millions of years.
In fact, they harbor unbalanced endemic fossil assemblages,
which would support both long isolation and sweepstake
immigrations (de Vos et al. 2007, Ali and Huber 2010,
van der Geer et al. 2010). The careful examination of the
seaﬂoor around islands such as Cyprus and Madagascar,
for example, shows the presence of structural highs (reliefs)
blanketed by as-yet-unexplored Quaternary sedimentary
successions (e.g., see the Deep Sea Drilling Project, www.
deepseadrilling.org/25/dsdp_toc.htm, which systematically
bypassed the Pleistocene deposits overlying the Davie Ridge,
which crosses the Mozambique Channel). From the lite-
rature, we learn, for instance, that the Plio-Pleistocene
terms of the stratigraphic sequences over the northeastern
underwater extension of the Kyrenia Mountains, at Cyprus,
are missing or largely condensed (Aksu et al. 2005), which
happens when a previously submerged structure surfaces.
The same literature indicates that those structures were also
affected by active Quaternary tectonics and volcanism. The
Quaternary is a time during which the sea level ﬂuctuated,
sometimes dropping 120–130 meters, in response to a cyclic
climatic forcing. We can speculate that the interplay of tec-
tonics and sea-level low stands may have temporarily created
connections with the nearest mainland, at least during the
most severe glacial periods, which would have favored the
colonization of those islands.
Biogeographic studies of the Galápagos Archipelago also
show how biogeographic models are often geologically depen-
dent. Geological consensus favors the oceanic origin of the
archipelago—that is, entirely volcanic and with a seaﬂoor
composed of oceanic plates (cf. Bowman et al. 1983). This
geological model allows only for overwater dispersal or for so
called stepping-stone colonization. Grehan (2001) reviewed
an alternative model, developed by Croizat (1958) and cor-
roborated by the plate tectonic solution proposed by Holden
and Deitz (1972): the Galápagos Gore. In this scenario, the
Galápagos biota would have been inherited from a whole
series of ancestral Galápagos Islands located on the eastern
Paciﬁc plate, which is called Cordilleria and which progres-
sively merged with North, South, and Central America
between the Mesozoic and the Cenozoic Eras.
Taphonomic sampling and analytical biases
Returning to the issue of unbalanced assemblages, not
all species fossilize with the same degree of detail or fre-
quency. The stratigraphic record of paleontological events is
highly dependent on taphonomic—fossilization—processes
( ﬁgure 1), and taphonomic biases exist against rare species
and species with a low potential of preservation (Lyman
1994). An insular fossil assemblage might in truth be
unbalanced because of preservational biases rather than
sweepstake colonization, or through a combination of these
factors. Moreover, rare species have a low chance of being
included in the fossil record (McKinney et al. 1996).
Carnivores are a case in point. The reason for which large
carnivores are apparently absent from insular fossil records
could be related to various factors. Carnivores are usually
rare in insular faunal communities; however, in areas in
which food abundance and space are limited and com-
petition is the most ﬁerce, as on islands, they are essentially
even rarer. In the fossil record, they virtually disappear. The
chances that carnivore bones, which are so statistically spo-
radic, can survive all potential post mortem destruction and
that a (rare) stratigraphic sequence can capture evidence
of them are, in fact, very low. Only the biostratinomic (i.e.,
post mortem and preburial) accumulation and concentra-
tion of carcasses and bones under certain conditions, such
as in natural conservation traps (e.g., caves or natural pits),
increase the probability of carnivore fossilization (Masseti
1995). In general, post mortem transport of the remains of
a taxon by biotic (e.g., carnivores, scavengers) or abiotic
agents (e.g., stream) to areas extraneous to its original habi-
tat is negligible (Kidwell and Holland 2002).
Temporal resolution and the usually heterogeneous pat-
terns of many fossil records contribute to the variability
of single stratigraphic successions and to the balanced or
unbalanced nature of a fossil assemblage. However, the
voids of information within each stratigraphic section can
be ﬁlled by combining paleontological data from mul-
tiple sections and sedimentary basins (Kidwell and Holland
2002). This would strengthen any colonization hypotheses.
But islands, being de facto a limited physical space, often
prevent such composition of paleontological data because
of the rarity of fossiliferous stratigraphic sequences, which
adds to the difﬁculty of reaching any ﬁrm conclusions.
Taphonomic analysis is further confounded by time
averaging, whereby animal remains may build up over
time through attrition, forming accumulations that mimic
natural communities. Kidwell and Behrensmeyer (1993)
showed that the time span represented in any fossil assem-
blage may vary over many orders of magnitude. The more a
fossil assemblage is attritional, the higher the probability is
that it is an artiﬁcial combination of communities from dis-
tinct climatic or sea-level change events scattered over time.
In order to reconstruct the ecological characters of insular
communities, the different colonizers must be treated as
having equal preservational potential, which is seldom—if
ever—the case, as was mentioned above. There follows a
strong desire in analyses of such insular communities to
disentangle these data and to establish their true ecological
characteristics—that is, the faunal interrelationships and
the degree of balance or unbalance and of diversity at any
one point in time. Despite the ﬂurry of studies on insular
endemic modiﬁcations, little attention has been paid to
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 943
methodological limitations and inaccuracies. Little research
has been devoted to the impact that insufﬁcient sampling
and inadequate sampling techniques, together with imper-
fect taxonomic determinations and improper data recording
during recovery, have had on the study of insular coloniza-
tion. How much do these biases weigh on the diagnosis of an
“unbalanced” fossil assemblage?
Climatological factors and eustatic evolution
Climate has a profound inﬂuence on the diversity pat-
terns of insular mammals. Because mammal communities
cannot quickly move off of islands, they are heavily affected
by climatic variation. Insular communities can withstand
only limited and slow changes, and species turnover is
signiﬁcantly higher than in continental mainland contexts
(Lomolino et al. 2010). Climate-driven selection can easily
lead to unbalanced insular land mammalian communities.
The contribution of paleoclimatology can also explain the
tempo and mode of the evolution of insular ecosystems in
general and of insular land mammal communities in par-
ticular (see ﬁgure 1).
The Quaternary was a time of frequent and intense climatic
change. During the Pliocene Epoch, the average tempera-
ture and humidity steadily dropped, because of alternat-
ing climatic conditions (see Sarnthein et al. 2009 and the
references therein). Environmental instability affected biotic
ecosystems. Climate-induced ecological release (the expan-
sion of habitat and resource use by certain species in areas
with lower diversity) can have serious consequences within
the restricted and sensitive settings of islands. An insu-
lar ecosystem can be variously restructured and renewed
in direct and relatively rapid response to climate change
Sea-level oscillations can create or destroy physical and
ecological connections and barriers, which can promote
habitat uniformity or fragmentation (see ﬁgure 2). In the
course of the Quaternary, extensive, climate-driven sea-
level variations had severe consequences for landform-
shaping processes. How the global sea level has changed
over time is now fairly well known (cf. Miller et al. 2005),
but the reconstruction of sea-level ﬂuctuations at more
local levels is still in the early research stages. Knowing
how paleogeographic settings varied in response to eustatic
changes (ﬁgure 1) is crucial to understanding how and
why mammal communities of continental islands started
and continued or disappeared over time. The often-clear
correlation between well-dated insular fossil communities
and sea-level variations could, in fact, be indicative of a
causal relationship, with eustatic events driving bio logical
ones (e.g., Madagascar; Warren et al. 2010). Coming to
Figure 2. The Mediterranean during the peak of the Last Glacial Maximum (approximately 18,000 years ago). The
example shows how common island connections to the mainland are during sea-level low stands. The dotted contour
represents the present-day Mediterranean coastline. Global, climate-driven sea-level variations and geological dynamics
can either open or close the way to islands. This regulates the inﬂux of land mammals on islands, with chain reactions
determining ecological settings, behavioral and physiological responses, population density patterns, and gene ﬂow.
Abbreviation: km, kilometers. Source: Adapted with permission from Thiede (1978).
944 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
ﬁrm conclusions about land mammal insular communities,
however, is often prevented by the stratigraphic uncertain-
ties of the fossil record in most island contexts. In many
instances, this kind of eustatic–fossil correlation would be
the deciding factor between alternative hypotheses of insular
The Quaternary Period includes 103 climatically driven
sea-level variations (Miller et al. 2005), some of which
greatly exceed 100 meters in magnitude. However, just how
often or to what extent have researchers cross- correlated
geological evidence from islands with these sea-level varia-
tions when trying to establish periods of connection with
mainland areas? And just how much has this geological and
eustatic history been compared with the paleontological
Ecological and physiological factors
The physiology, ecological dynamics, and environmental
choices of land mammals in insular settings are the areas
most investigated by (paleo)biogeographers and paleon-
tologists in their search to understand dynamic evolutionary
processes on islands, but they are also the topics that have
provoked the most heated debate. The results of decades of
insular-ecosystem research clearly show that various eco-
logical causes account for the unbalanced character of many
living insular mammalian communities (Palombo 2009b).
Paleontologists could beneﬁt from this invaluable informa-
tion by concluding that unbalanced fossil insular mamma-
lian communities are not necessarily the indisputable result
of sweepstake colonization.
Island colonization, an ecologically selective phenomenon. Ecologists
can help to show that island colonization and the composi-
tion of insular communities or assemblages are governed
by a high level of natural selection and species extinction.
Different levels of susceptibility to extinction, abilities to
migrate, and other vulnerabilities or capabilities can lead
to different responses in and among species in insular
settings (Lawlor 1986). Relaxed community fossil assem-
blages (Brown JH 1971) are those in which a species’ rich-
ness decreased over time, as, for example, when the more
resource-demanding taxa (e.g., large specialist carnivores)
became extinct, which would have allowed smaller-sized
generalists to develop higher population densities. Different
levels of vagility, vulnerability, and susceptibility to extinc-
tion can lead to different responses among species in insular
settings (e.g., Lawlor 1986). An example is offered by the
rapid disappearance of over 75% of the original vertebrate
species from the small- and medium-size islands that were
created by the ﬂooding of the mountainous areas of Panama
when the Panama Canal was opened (Terborgh 1974).
Some paleontologists relate the selection of species that
can be found on islands to those species’ swimming skills
and have argued that the presence or absence of speciﬁc
ungulates in insular fossil assemblages is a result thereof (see
de Vos et al. 2007 and the references therein, van den Hoek
Ostende et al. 2009). Taxa not normally found on islands
either today or in the past, such as perissodactyls, are deemed
to be poor or short-distance swimmers (de Vos et al. 2007).
In contrast, cervids (e.g., giant deer or red deer), which are
frequently found in insular fossil communities, are consid-
ered to be good and long-distance swimmers. In spite of the
fact that ecoethologists can give valuable information about
the swimming abilities of the living counterparts of past
land mammals (see below), the presence or absence of land
mammals on islands may very well depend on the vagaries
of climate change, as well as on the island’s resources, size,
degree of isolation, and microclimatic conditions. However,
perhaps most important is the vegetation at the supposed
time of colonization and thereafter. Opportunistic feeders,
including red deer and goats (e.g., Myotragus), are selec-
tively favored as island colonists over concentrate selectors,
such as large bovids, and grass and roughage eaters, such
as equids (e.g., Hofmann 1989). This may explain why
Megaceroid deer, red deer, and goats are (or were) so suc-
cessful on islands, whereas roe deer, horses, and large bovids
are (or were) so rare or thoroughly absent.
Equids may also be absent from islands for other rea-
sons. Wetlands and thick, humid tropical rainforests, such
as those of southeast Asian archipelagos, act as ecologic
ﬁlters, keeping out equids but admitting certain kinds of
rhino ceroses. In fact, forest-dwelling rhinoceroses estab-
lished on Luzon (Philippines), possibly from Indochina,
and on the Japanese islands. During Late Pleistocene sea
low stands, these islands were connected repeatedly with
the mainland and could easily be reached by roaming rhi-
noceroses. Convoluted explanations of island colonization
based on animal buoyancy or swimming skills enhanced by
intestinal gasses (de Vos et al. 2007) could easily be avoided
by closer collaboration among paleontologists, geologists,
paleo climatologists, and ecologists, as we have said before.
Another erroneous attribution of causality, again through
a lack of cross-disciplinary reference, is the widely held
belief—due to the absence of large carnivores—that many
fossil insular assemblages are highly unbalanced (e.g., de Vos
et al. 2007, van den Hoek Ostende et al. 2009), despite the
hard evidence that the number of different species of insular
carnivores—large ones included—is considerable (table 2).
Islands with wetlands and intricate, humid tropical rain-
forests are indeed unsuitable for social carnivores, such as
canids and lions, who need vast expanses of physical territory
in order to ensure the survival of a minimum population size.
Nonetheless, forests are the ideal habitat for solitary ambush
predators, such as jaguars, leopards, and tigers; although
leopards and tigers do reach islands covered with forests
(table 2), felids seem to have never undergone endemic modi-
ﬁcations on islands. In fact, the differences between insular
felids and their mainland ancestors never range beyond
the subspeciﬁc level—for example, the Japanese Iriomote
cat (Prionailurus bengalensis irio motensis) and Tsushima cat
(Prionailurus bengalensis euptilura) are still genetically close
to the continental leopard cat (Prionailurus bengalensis;
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 945
Masuda and Yoshida 1995). Once again, neontological data
can show that more resource-demanding hypercarnivores
(i.e., those with more than 70% of their diet consisting of
meat) are more vulnerable on islands than are meso- (meat
between 50% and 70% of their diet) and hypocarnivores
(meat less than 50% of their diet) and that they rapidly dis-
appear (O’Regan et al. 2002).
Faunal interaction. Species interaction is yet another fruitful
area for research into past insular land mammals. Studies of
insular ecology have been focused particularly on competi-
tion (e.g., Raia and Meiri 2006), as opposed to parasitism,
predation, or mutualism. However, the former is not always
the deciding factor in the ecology of larger, more hetero-
genous islands: Research shows that these islands tend to
carry more-diverse biotas than do smaller islands with eco-
logically similar species peaceably occupying distinct and
separate areas, as in a checkerboard conﬁguration (Diamond
1975). Large islands can offer essential space to pioneer spe-
cies that then create new niches for other potential immi-
grants (Lomolino et al. 2010). However, competition could
be the reason that ecologically similar species do not often
coexist on smaller islands. Species interaction can limit bio-
diversity and may result in impoverished and probably also
unbalanced communities but can also create new chances
for evolution for certain species. In addition, habitat frag-
mentation, whether within larger islands or between islands,
greatly affects immigration and extinction patterns, increas-
ing or reducing colonization success. Ecological studies are
therefore another valuable resource in the interpretation of
insular fossil records.
Natural rafting, a still unexplored solution. Overseas dispersal
by natural rafting is often advocated to explain biogeographic
conundrums—that is, the bafﬂing presence of vertebrates,
invertebrates, and some plants, especially of salt-intolerant
taxa, on oceanic or oceanic-like islands (cf. Ali and Huber
2010). The idea is that violent storms might have dislodged
large masses of vegetation that were then carried down rivers
and out to sea, forming temporary islands on which animals
could take refuge. Dispersal then required favorable currents
by which species rapidly traversed stretches of saltwater. This
kind of sweepstake dispersal theory is currently enjoying
vast popularity and has been readily embraced—perhaps
too enthusiastically—by both neontologists and paleontolo-
gists. In fact, doubts are starting to emerge (Stankiewicz et al.
2006, Masters et al. 2007). How much attention is paid to the
actual physical and physiological characteristics and capaci-
ties of land mammals? Crossing oceanic stretches would
expose them to large temperature and humidity variations,
to high concentrations of salt, and—more problematic for
land mammals—to a prolonged lack of food and water. We
can suppose that they traveled in torpor or in states of hiber-
nation and, therefore, at metabolic levels lower than nor-
mal (Ali and Huber 2010). However, not all mammals are
capable of lowering their metabolic levels to any signiﬁcant
degree, nor of spontaneously arising from metabolic torpor
when conditions change. Terrestrial mammals, especially
larger ones, are at a disadvantage relative to other animals
because of their high energy requirements. In contrast,
they are more effective thermoregulators than poikilotherm
animals (i.e., those with variable body temperature) and
smaller mammals and can therefore cope with temperature
instability more effectively (Masters et al. 2007). Moreover,
terrestrial mammals rafting across sea straits would need to
do so in sufﬁcient numbers to successfully colonize an island
over time. Small colonizing populations are more sensitive
to genetic drift and show increased inbreeding and relatively
low genetic variability. There is a critical number of indi-
viduals required to avoid extinction or the unsteadiness of
genetic drift (Reed et al. 2003).
Accounts of land mammals observed on ﬂoating mats of
vegetation are rare and, in most cases, anecdotal. Monkeys
and rodents have been seen on ﬂoating debris in rivers (van
Duzer 2004), where drinkable water is readily accessible,
unlike under sea conditions. How long would those ani-
mals survive in transoceanic dispersal? Prescott (1959)
reported the case of a jackrabbit (Lepus californicus) found
perched on a pelagic raft of giant kelp (Macrocystis pyrifera)
some 24 kilometers (km) southeast of one of the three
Channel Islands off the coast of San Clemente, California.
The animal was in a very poor condition. This is the only
account available in the literature in which a terrestrial
mammal was observed to be traveling on ﬂotsam across a
stretch of seawater. Moreover, this example actually speaks
against island colonization through natural rafting in that
no jackrabbits are reported to inhabit any of the Channel
Islands, despite the fact that L. californicus has been present
Table 2. Insular carnivores.
Arctic islands Ursus maritimusb, Vulpes lagopusc
Mediterranean islands Chasmaportetes meleib, Cynotherium
sardousc, Crocuta crocutab, Canis lupusc,
Ursus arctosb, Panthera leob, Canis aureusc,
Vulpes vulpesc, Martes mar tesc, Martes
foinac, Meles melesc, Mustela nivalisc,
Lutra lutrac, Enhjidrictis galictoidesc,
MadagascaraFossa fossanac, Eupleres goudotiic,
Galidia elegansc, Galidictis fasciatac,
Mungotictis lineatusc, Salanoia concolorc,
Zanzibar Panthera pardus adersib
Southeast Asian islands Prionailurus viverrinusb, Prionailurus
bengalensisb, Neofelis nebulosab,
Panthera pardusb, Panthera tigrisb
Japanese islands Prionailurus bengalensis iriomotensisb,
Prionailurus bengalensis euptilurab
Falkland islands Lycalopex griseusc
aAll from a single colonization event. bHypercarnivore.
946 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
in western North America since the early Irvingtonian Age,
over 1.5 million years ago (Barnosky 2004). In all this time,
rafting jackrabbits have never colonized any one of the
three Channel Islands, which are located, at most, 120 km
off the California coast.
Natural rafting raises many more problems than it solves.
Accurate integrated ecoethological and physiological tests;
population genetics studies; and geological, paleogeographic,
and paleooceanographic reconstructions are required before
rafting can be proposed as a plausible hypothesis for the
colonization of islands at any distance.
Behavioral factors: Swimming to colonize
Climatic changes and ecological contexts need to be care-
fully deﬁned before any conclusions are reached about their
impact on animal behavior; in fact, these changes can be
environmentally dependent (ﬁgure 1) and can be medi-
ated by epigenetic mechanisms (Ledón-Rettig et al. 2013).
Rapid epigenetic behavioral variation facilitates population
survival wherever environmental change is too rapid for
genetic modiﬁcation to arise. This is therefore an important
adaptive resource under unstable and rapidly changing envi-
ronmental conditions, such as on islands.
Such models of animal behavior form the basis of many
hypotheses of island colonization through overwater dis-
persal. However, the swimming skills and propensity to
venture into water of many land mammals are sometimes
overrated or inaccurately represented. Although substantial
bodies of water can occasionally be accidentally crossed
by one-way sweepstake dispersers, as in the case of natural
rafting, they normally act as ﬁltering passages—technically,
pendel routes, which can be crossed in both directions only
by good swimmers (Dermitzakis and Sondaar 1978) or
by animals predisposed to venture into water. Swimming
is neither easy nor natural for most terrestrial mammals,
although most can swim after a fashion. It would follow that
any swimming or behavioral hypotheses would signiﬁcantly
beneﬁt from a minimal cross-checking with ecoethologists.
Cervids and elephants are capable swimmers, however.
Thanks to their streamlined body shape, cervids are poten-
tially more agile swimmers than elephants are (Held 1989).
However, empirical observations reveal that deer do not
swim very often (Vigne and Marinval-Vigne 1988) and
cannot swim long distances—only managing a consecutive
2–3 km swim, on average (Brown D 2005)—and need to
have the opposite shore within sight (Severinghaus and
Cheatum 1956). Cervids whose swimming performance has
been reported in the literature are always at least as large as
Elephants, however, seem to be able to swim almost 50 km
(Johnson 1980), owing to their unique lung anatomy, while
using their trunks for snorkeling (West 2001). Because
they tend to swim in herds, elephants can reach islands in
relatively high numbers and can therefore form sufﬁciently
varied gene pools, which increases the chances of successful
colonization (see below).
Suids seem to be proﬁcient swimmers (Oliver et al. 1993).
Whether hippopotamuses can swim or even ﬂoat is another
issue of contention. Many researchers (Marra 2005, Ali and
Huber 2010) consider them excellent divers and swimmers
in view of their aquatic lifestyle. However, according to
earlier studies (e.g., Eltringham 1999, Fisher et al. 2007) and
more recent studies (Coughlin and Fish 2009), hippopota-
muses do not swim at all. The structure of a hippopotamus’s
body seems to be designed to overcome buoyancy, which
helps it keep its feet ﬁrmly stuck to the water bottom while
also preventing its barrel-shape body from rolling, thus
avoiding unstable motion (see Coughlin and Fish 2009 and
the references therein).
Another factor mitigating against any kind of oceanic
crossing by hippopotamuses is that they naturally avoid
deep water. Under normal circumstances, juveniles resurface
to breathe every 2–3 minutes and adults every 3–5 minutes
(Eltringham 1999). They also do this automatically when
sleeping underwater (Jackson and Gartlan 1965). The hydro-
static pressure in deep water would prevent this behavior.
Supposing that hippopotamuses cannot swim, a pos-
sible alternative to explain their presence on islands is that
of passive transportation by rafting, but this hypothesis is
highly implausible, for a number of reasons. Adult hippo-
potamuses weigh from 1.5 to 3 metric tons: How thick does
a tangled mat of vegetation need to be to act as a sea worthy
raft to carry several individuals of this size? Moreover,
hippo potamuses need to drink large amounts of water daily
(Calder 1984) and are very sensitive to exposure to solar
Hippopotamuses reached land-bridge islands, such as
the British Isles, Sicily, Malta, and Maﬁa. In the course
of the Quaternary, temporary connections between land-
bridge islands and their nearest mainland areas were
recurrently created by the favorable interplay of regional
uplifts, glacioisostatic rebounds, and high-amplitude glacio-
eustatic changes. But hippopotamuses also colonized Crete,
Cyprus, and Madagascar, which are classiﬁed as oceanic or
oceanic-like islands (e.g., van der Geer et al. 2010). If hippo-
potamuses cannot swim, oceanic island colonizations are
difﬁcult to explain. In the absence of a credible alternative
explanation, the presence of hippopotamuses on islands
suggests the existence of (perhaps ﬁltering but walkable)
land-bridge connections. Here, we can see how the adoption
of a multi- and interdisciplinary approach is essential to
understanding events in their full complexity.
Large terrestrial carnivores are absent from unbalanced
insular faunas. For this reason, some scholars consider those
species poor swimmers (de Vos et al. 2007, van den Hoek
Ostende et al. 2009). The numerous sightings and fossil
records of carnivores on islands would seem to contradict
this opinion (table 2). Leopards and tigers have been repeat-
edly sighted in southeastern Asian islands, as was mentioned
As has already been discussed, the lack of large carnivores
from insular faunal or fossil records can be explained by
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 947
ecological incompatibilities, as was predicted by the relax-
ation theory, or by preservational biases, as in the case of
fossil assemblages, in which some kinds of animal remains
have low probabilities of being preserved by rare insular
stratigraphic successions (O’Regan et al. 2002). In these
cases, swimming abilities or their absence in these animals
are not part of the bigger picture.
Small mammals are often good but short-distance swim-
mers. Empirical observations indicate that rodents normally
swim, at most, only few hundred meters, with the exception
of Norway rats and red squirrels, which can swim up to
2 km (Russell and Clout 2005, Fritts 2007). Rodents cannot
reasonably be expected have crossed the 972 km of ocean
range separating the Galápagos Archipelago from Ecuador’s
shoreline (van den Hoek Ostende et al. 2009). It seems
therefore unrealistic to posit that short-distance-swimming
micromammals colonized the Galápagos Islands through
stepping-stone immigration and even less so through natu-
ral rafting. Furthermore, the difﬁculties of reaching any ﬁrm
conclusions about the colonization of the Galápagos Islands
are compounded by the commonly held assumption that
they are of oceanic origin, as was explained above. This is
another example in which coordinated multi- and inter-
disciplinary research among scientists could be a recipro-
cally rewarding approach.
But what drives terrestrial animals into an alien envi-
ronment such as water? Density-dependent factors, such
as competition, the search for food and partners, or—
conversely—predation (see Lomolino et al. 2010 and the
references therein) seem to be logical factors. However,
attempts to evade capture, predators, and aggressive con-
speciﬁcs or ﬂight from ﬂoods or ﬁres may also be relevant,
but random events and sheer chance could, in many cases,
be the real reasons for animals’ venturing into water in
search of new territories (Severinghaus and Cheatum 1956,
Brown D 2005).
Genetics and densities of colonizing populations
Unstable factors and circumstances affect the population
size and density of any group of animals, and these effects
are hard to quantify, especially post hoc, in fossil assemblages.
Furthermore, in any ecological environment, the number
of conspeciﬁcs, population density, and individual ﬁtness
are dynamically interrelated (i.e., the Allee effect; Stephens
et al. 1999) and correlate with an environment’s carrying
capacity (ﬁgure 1; Barton and Turelli 2011). The subtle
interplay of these parameters establishes the critical density
threshold under which a population is doomed to extinction
and above which it can increase deterministically (Barton
and Turelli 2011). A small colonizing population is more
sensitive to environmental and demographic stochasticity
(random unsteadiness; Stephens et al. 1999). A population
of land mammals might theoretically accumulate on an
island through successive colonizations, but the length of
time that would be required to ensure stable colonization
would be far too long. The maximum number of individuals
that can live on an island is determined by the island’s car-
rying capacity, which varies.
It follows that terrestrial mammals can become estab-
lished on an island only if they arrive in sufﬁcient numbers
and if the circumstances on the island allow for a local
deterministic increase in population. Quite naturally, any
population of colonizers that detaches from a larger main-
land population experiences a loss of genetic variation (i.e.,
Mayr’s 1942 founder effect) and diverges from the mainland
population both genetically and phenotypically. The colo-
nizers also show increased inbreeding.
Excluding freely accessible, two-way corridor bridges, a
key issue that needs to be addressed jointly by genetists,
biogeographers, and paleontologists is whether ﬁltering
corridors and sweepstake modes of immigration allow for
the passage of a sufﬁcient critical number of individuals
to ensure the survival of colonizing species. To successfully
colonize an island, a swimming taxon needs not only to be
a good swimmer, predisposed to venturing into water, but
also to be an r-strategist (i.e., it must have high reproductive
potential and a limited or no requirement for parental care).
Deer, hippopotamuses, and elephants, which are found on
many islands around the world, are K-selected animals (i.e.,
they produce fewer offspring and often practice extensive
parental care; Eltringham 1999, Moore 2007). This suggests
that individuals in insular settings probably undergo (per-
haps genetic) changes that collectively contribute to main-
taining sufﬁciently varied gene pools or to increasing genetic
variability. Apparently, settlements on islands may be con-
solidated by transitions from a K-strategy to an r-strategy
(in the early stages of colonization) and then back to a
K-strategy (i.e., specialization and low birth rate; Lomolino
et al. 2010).
At the initial stages of colonization, very small popula-
tions of immigrants are sensitive to environmental and
demographic unsteadiness, but the endemic modiﬁcations
shown by insular invaders are strikingly recurrent. Insular
species’ body size is constrained by multiple complex fac-
tors (Meiri 2007). Ecological release (i.e., the introduction of
a taxon to an environment other than its original habitat)
typically promotes gigantism in small vertebrates (McNab
1994). In contrast, resource limitation promotes dwarﬁsm
in large-size taxa (Anderson and Handley 2002). Therefore,
these seem not to be random but, rather, channelized evo-
lutionary processes; that is, they are strongly constrained
by functional and adaptive limitations and perhaps also by
morphogenetic or constructional and phylogenetic conﬁne-
ments. Millien and Damuth (2004) cite examples that result
from geographical conﬁnement and limited resources, in
line with Van Valen’s (1973) island rule (according to which
large species on islands tend to become nanoid, whereas
small ones become gigantic).
In analyzing the relationship between body size and
distribution patterns, Marquet and Taper (1998) observed
that both large- and small-size species with low density and
highly variable body size are best adapted to large territories
948 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
and are at greater risk of extinction in smaller ones. However,
medium-size species (of about 100 kilograms) are able to
form denser populations in smaller areas and are better able
to adapt to islands, in general. Therefore, smaller islands best
support only medium-size animals. These considerations
led Marquet and Taper (1998) to state that the average body
size of a species can indicate the minimum area it needs for
survival. Large terrestrial mammals rapidly evolve to lose
size and reduce their energy needs on islands and, there-
fore, increase their chances of survival (McNab 1994). For
the reason explained above, equids do not spontaneously
colonize islands by crossing water straits, but some human-
introduced equids have developed dwarf representatives
in insular contexts. Domestic horses and donkeys became
smaller after their introduction onto some Mediterranean
islands (cf. Masseti 2002).
Large mammal species that evolve smaller body sizes
and reduce their resource requirements can produce larger
and denser populations, thereby gaining gene-pool rich-
ness and eventually lowering their risk of extinction. In
contrast, by reducing reproductive output and growing in
body size (Adler and Levins 1994), smaller mammals lower
their mass-speciﬁc maintenance costs. Because of their com-
paratively higher body surface-area:volume ratio, smaller
individuals necessitate a high energy intake to maintain
body heat (Calder 1984). Therefore, having migrated onto
islands, individuals of species that are usually of large or
small size in mainland areas converge toward ideal medium
sizes (Millien and Damuth 2004). A corollary to these con-
clusions is that, being more protected from the uncertainties
of the environment by their denser populations, but also by
their potentially richer and more varied gene pools, terres-
trial mammals living in ﬂocks are expected to be somewhat
more successful in colonizing islands than more solitary taxa
The conclusion of this reasoning is that, in order to favor
the necessary adaptations to insular conditions and assure
community survival, land mammals need to colonize islands
with a critical and substantial number of individuals. The
question is whether a sweepstake process of immigration
could ever ensure those numbers.
The analysis of the spatial distribution of genotypes and
of genealogical lineages needs to be based on phylogenetic
analysis. The resulting phylogenies, or evolutionary histories,
are constructed from genetically controlled features, such as
morphology or behavior, and from gene-sequence analysis.
Gene-sequence analysis provides the basis for determin-
ing phylogenetic relationships and morphology: It drives
many neontologist models, including the calculation of
the timing of colonizations and the evolutionary and eco-
logical interactions between colonizing and resident spe-
cies. However, phylogeographical inferences with limited
or no paleontological, geological, and paleoclimatological
veriﬁcation might lead to highly controversial conclusions
(e.g., such as those in Pulquério and Nichols 2007, which
showed great discrepancies in the dates of evolutionary
events obtained using the molecular clock). Paleoecology,
which outlines the habitat requirements of colonizing spe-
cies (ﬁgure 1), is a particularly important aid to phylogeo-
graphers. All of these disciplines play a key role in providing
the historical framework for reliably interpreting relation-
ships among molecular sequences.
More recent history can help supply paradigms for and
help formulate the reconstruction of insular coloniza-
tion events. Occasionally and unexpectedly, historical and
documentary sources from museum collections or zoo-
archeological data can supply crucial information to under-
stand otherwise inexplicable occurrences or biotic changes
on islands. It is well known that many pests (such as mice
and rats) were involuntarily introduced onto islands by
human colonizers. Through Varro (De re rustica 3.12.1),
for example, we know that releasing hares on islands was
an ancient Roman practice that was maintained up to his
time in the so-called leporaria. Animals were introduced
on islands to create game parks. This was still customary
during the Middle Ages, when sailing ships distributed rab-
bits on islands as a source of food for sailors (McNitt et al.
2000). The introduction of alien organisms onto islands by
humans may have often been signiﬁcantly ecologically dis-
ruptive (Courchamp et al. 2003); it is, however, relatively
easy to reconstruct.
We cannot exclude the possibility that answers to some
biogeographic conundrums might lie buried in neglected
historical records and might be related to intentional or acci-
dental human-mediated faunal translocations. Therefore,
collaboration with historians could be another important
approach in this ﬁeld. The historical biogeography of insu-
lar land mammals is, in our view, one of the most prom-
ising directions for future multi- and interdisciplinary
research and a key area for probable breakthroughs and
As we have seen, islands and insular faunas and fossil assem-
blages develop as the result of a complex range of inter-
connected events, conditions, and processes. Insular speciation,
itself, and rates of immigration or of extinction of insular
biomes, ecosystems, and communities are often greatly
inﬂuenced, not just by the geological, geomorphological,
and geographic evolution of islands but also by eustatic
ﬂuctuations, changing climatic and ecological conditions,
and epigenetically driven behavioral changes.
Because this network of intricate interdependent variables
needs to be deﬁned and analyzed, it would seem impera-
tive that any study of insular community characteristics or
any reconstructions of the processes of insular community
formation would need to encompass large-scale, evidence-
based, multidisciplinary approaches.
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 949
Indispensable starting points from which to detect pos-
sible biases in the relevant data sets are often initially deter-
mined both by detailed taphonomic screening and by solid
stratigraphic analysis. The conﬂuence of paleontology and
geology is essential in revealing the chronological constraints
that might impinge on the duration of particular bone beds
and in ascertaining the uniformity of the assemblages
themselves. This cross-referencing ultimately allows for the
evaluation of the reliability and strength of different data.
The dating of biological events—that is, the biochronology
of succession of endemic fossil assemblages—is, further-
more, very useful in a wider context, to geologists who are
trying to determine the interrelations between different
structural units within any geological succession. Similarly,
unraveling the geological and geographic history of islands,
as well as revealing and dating their possible relationships
with mainland areas, is as important to paleontologists as it
is to biogeographers. Learning whether a piece of land has
always been isolated or whether and when that land ceased
to be an island is crucial in establishing the origin and
development of insular communities. It would follow that
the other disciplines mentioned in this study intersect with
and enhance each other in similar ways. For example, cross-
checking the geological evolution of islands with sea-level
variations can reveal previously undetected island–mainland
connections. Climate-driven eustatic sea-level changes, in
turn, inﬂuence the development and disturbances of insu-
lar ecosystems. Knowing the prevailing climatic conditions
at any point in time and cross-referencing this informa-
tion with the ecological preferences of the inhabitants of
islands may explain species discontinuities already indi-
cated by nonuniform assemblages. Geologists, paleontolo-
gists, taphonomists, stratigraphers, paleoclimatologists, and
paleooceanographers, therefore, all potentially contribute to
the building of a historical framework for the most-effective
neontological research on insular mammals. However, biolo-
gists, biogeographers, ecoethologists, and geneticists provide
comprehensive data sets on the behavioral and physiological
features of particular species, their ecological characteristics
and environmental choices and possible ecological inter-
actions, their genetic compositions and epigenetic changes,
and their phylogenetic relationships. More recent data, both
historical and current, on the population dynamics of extant
natural insular terrestrial mammal communities and of liv-
ing counterparts of previously insular faunas or of extant
equivalents of past taxa provide a solid foundation and theo-
retical testing ground for paleobiological reconstructions,
hypotheses, and colonization models.
Researchers of islands are therefore confronted by a
tangled network of related variables, which, quite naturally,
points toward the study of each island, past or present, on
a case-by-case basis. It would seem inevitable that conclu-
sions of a generalizing nature would inevitably be made
from such studies. Nevertheless, some caution should be
exercised, in that these conclusions should be reached only
after at least some or possibly many of the above-discussed
factors and aspects have been thoroughly investigated and
either discounted or incorporated.
The strength, credibility, and applicability of our recon-
structions of insular evolution and colonization are strongly
dependent on the solidity of data sets. Ignoring such a
heuristic principle may produce a split in the scientiﬁc com-
munity between those who tend to rely on models and those
who believe that empirical evidence is the only “true” source
of information, whereas, in fact, as with disciplinary cross-
fertilization, a mixture of the two approaches is needed in
We are greatly indebted to Marco Festa-Bianchet and Adrian
Lister for their invaluable advice and assistance. A previous
draft also beneﬁted from the critical reading of Shai Meiri.
We also thank Kate Eadie for the language editing. This
study was ﬁnancially supported by PRIN (Research Projects
of National Interest) 2009 MIUR (the Italian Ministry of
Education, University and Research) grants.
Adler GH, Levins R. 1994. The island syndrome in rodent populations.
Quarterly Review of Biology 69: 473–490.
Aksu AE, Calon TJ, Hall J, Mansﬁeld S, Yaşar D. 2005. The Cilicia–Adana
Basin complex, Eastern Mediterranean: Neogene evolution of an active
fore-arc basin in an obliquely convergent margin. Marine Geology 221:
Ali JR, Huber M. 2010. Mammalian biodiversity on Madagascar controlled
by ocean currents. Nature 463: 653–656.
Anderson RP, Handley CO Jr. 2002. Dwarﬁsm in insular sloths: Biogeogra-
phy, selection, and evolutionary rate. Evolution 56: 1045–1058.
Barnosky AD, ed. 2004. Biodiversity Response to Climate Change in
the Middle Pleistocene: The Porcupine Cave Fauna from Colorado.
University of California Press.
Barton NH, Turelli M. 2011. Spatial waves of advance with bistable dynam-
ics: Cytoplasmic and genetic analogues of Allee effects. American
Naturalist 178: E48–E75.
Bowman RI, Berson M, Leviton AE. 1983. Patterns of Evolution in
Galapagos Organisms. American Association for the Advancement of
Brown D. 2005. Secretary Island Deer Eradication. Southland Conservancy,
New Zealand Department of Conservation.
Brown JH. 1971. Mammals on mountaintops: Nonequilibrium insular bio-
geography. American Naturalist 105: 467–478.
Calder WA III. 1984. Size, Function, and Life History. Harvard University
Coughlin BL, Fish FE. 2009. Hippopotamus underwater locomotion:
Reduced gravity movements for a massive mammal. Journal of Mam-
malogy 90: 675–679.
Courchamp F, Chapuis J-L, Pascal M. 2003. Mammal invaders on islands:
Impact, control and control impact. Biological Reviews 78: 347–383.
Croizat L. 1958. Panbiogeography. Published by the author.
Darwin C. 1859. On the Origin of Species by Means of Natural Selection,
or the Preservation of Favoured Races in the Struggle for Life. John
Dermitzakis MD, Sondaar PY. 1978. The importance of fossil mam-
mals in reconstructing palaeogeography with special reference to the
Pleistocene Aegean Archipelago. Annales Géologiques des Pays Hellé-
niques 29: 808–840.
De Vos J, van den Hoek Ostende LW, van den Bergh GD. 2007. Patterns
in insular evolution of mammals: A key to island palaeogeography.
950 BioScience • December 2013 / Vol. 63 No. 12 www.biosciencemag.org
Pages 315–345 in Renema W, ed. Biogeography, Time, and Place: Dis-
tributions, Barriers, and Islands. Springer.
Diamond JM. 1975. Assembly of species communities. Pages 342–444 in
Cody ML, Diamond JM, eds. Ecology and Evolution of Communities.
Harvard University Press.
Eltringham SK. 1999. The Hippos: Natural History and Conservation.
Fisher RE, Scott KM, Naples VL. 2007. Forelimb myology of the pygmy
hippopotamus (Choeropsis liberiensis). Anatomical Record 290: 673–693.
Fritts EI. 2007. Wildlife and People at Risk: A Plan to Keep Rats out of
Alaska. Alaska Department of Fish and Game.
Grande L. 1990. Vicariance biogeography. Pages 448–451 in Briggs DEG,
Crowther PR, eds. Paleobiology: A Synthesis. Blackwell Scientiﬁc.
Grehan J. 2001. Biogeography and evolution of the Galapagos: Integration
of the biological and geological evidence. Biological Journal of the
Linnean Society 74: 267–287.
Held SO. 1989. Early Prehistoric Islands Archaeology in Cyprus: Conﬁgu-
rations of Formative Culture Growth from the Pleistocene–Holocene
Boundary to the Mid-3rd Millennium B.C. PhD dissertation. University
Hofmann RR. 1989. Evolutionary steps of ecophysiological adaptation
and diversiﬁcation of ruminants: A comparative view of their digestive
system. Oecologia 78: 443–457.
Holden JC, Dietz RS. 1972. Galapagos Gore, NazCoPac Triple Junction and
Carnegi/Cocos Ridges. Nature 235: 266–269.
Jackson G, Gartlan JS. 1965. The ﬂora and fauna of Lolui Island, Lake
Victoria: A study of vegetation, men and monkeys. Journal of Ecology
Johnson DL. 1980. Problems in the land vertebrate zoogeography of certain
islands and the swimming powers of elephants. Journal of Biogeogra-
phy 7: 383–398.
Kidwell SM, Behrensmeyer AK. 1993. Taphonomic Approaches to Time
Resolution in Fossil Assemblages. Short Courses in Paleontology,
vol. 6. Paleontological Society.
Kidwell SM, Holland SM. 2002. The quality of the fossil record: Implica-
tions for evolutionary analyses. Annual Review of Ecology and System-
atics 33: 561–588.
Lawlor TE. 1986. Comparative biogeography of mammals on islands.
Biological Journal of the Linnean Society 28: 99–125.
Ledón-Rettig CC, Richards CL, Martin LB. 2013. A place for behavior in
ecological epigenetics. Behavioral Ecology 24: 329–330.
Lomolino MV, Riddle BR, Whittaker RJ, Brown JH. 2010. Biogeography,
4th ed. Sinauer.
Lyman RL. 1994. Vertebrate Taphonomy. Cambridge University Press.
McKenna MC. 1973. Sweepstakes, ﬁlters, corridors, Noah’s arks, and
beached viking funeral ships in palaeogeography. Pages 295–308 in
Tarling DH, Runcorn SK, eds. Implications of Continental Drift to the
Earth Sciences, vol. 1. Academic Press.
McKinney ML, Lockwood JL, Frederick DR. 1996. Does ecosystem and
evolutionary stability include rare species? Palaeogeography, Palaeo-
climatology, Palaeoecology 127: 191–207.
McNab BK. 1994. Resource use and the survival of land and freshwater ver-
tebrates on oceanic islands. American Naturalist 144: 643–660.
Marquet PA, Taper ML. 1998. On size and area: Patterns in body size
extremes across landmasses. Evolutionary Ecology 12: 127–139.
Marra AC. 2005. Pleistocene mammals of Mediterranean islands. Quater-
nary International 129: 5–14.
Masini F, Bonﬁglio L, Abbazzi L, Delﬁno M, Fanfani F, Ferretti M,
Kotsakis A, Petruso D, Marra AC, Torre D. 2002. Vertebrate assemblages
of central-western Mediterranean islands during the Pliocene and Qua-
ternary: Reﬂecting on extinction events. Pages 437–444 in Waldren WH,
Ensenyat JA, eds. World Islands in Prehistory: International Insular
Masseti M. 1995. Quaternary biogeography of the Mustelidae family on the
Mediterranean islands. Hystrix 7: 17–34.
———. 2002. Uomini e (Non Solo) Topi: Gli Animali Domestici e la Fauna
Antropocora. Florence University Press.
Masters JC, Lovegrove BG, de Wit MJ. 2007. Eyes wide shut: Can hypo-
metabolism really explain the primate colonization of Madagascar?
Journal of Biogeography 34: 31–37.
Masuda R, Yoshida MC. 1995. Two Japanese wildcats, the Tsushima cat
and the Iriomote cat, show the same mitochondrial DNA lineage as the
leopard cat Felis bengalensis. Zoological Science 12: 655–659.
Matthew WD. 1939. Climate and Evolution, 2nd ed. Special Publications
of the New York Academy of Sciences.
Mayr E. 1942. Systematics and the Origin of Species: From the Viewpoint
of a Zoologist. Columbia University Press.
McNitt JI, Patton NM, Lukefahr SD, Cheeke PR. 2000. Rabbit Production,
8th ed. Interstate.
Meiri S. 2007. Size evolution in island lizards. Global Ecology and
Biogeography 16: 702–708.
Miller KG, Kominz MA, Browning JV, Wright JD, Mountain GS, Katz
ME, Sugarman PJ, Cramer BS, Christie-Blick N, Pekar SF. 2005. The
Phanerozoic record of global sea-level change. Science 310: 1293–1298.
Millien V, Damuth J. 2004. Climate change and size evolution in an
island rodent species: New perspectives on the island rule. Evolution
Moore GS. 2007. Living with the Earth: Concepts in Environmental Health
Science, 3rd ed. Lewis.
Oliver WLR, Cox CR, Groves CP. 1993. The Philippine Warty Pigs
(Sus philippensis and S. cebifrons). Pages 145–154 in Oliver WLR, ed.
Pigs, Peccaries, and Hippos: Status Survey and Conservation Action
Plan. International Union for Conservation of Nature.
O’Regan HJ, Turner A, Wilkinson DM. 2002. European Quaternary refugia:
A factor in large carnivore extinction? Journal of Quaternary Science
Palombo MR. 2009a. Biochronology, palaeobiogeography and faunal
turnover in western Mediterranean Cenozoic mammals. Integrative
Zoology 4: 367–386.
———. 2009b. Body size structure of Pleistocene mammalian communi-
ties: What support is there for the “island rule”? Integrative Zoology
Prescott JH. 1959. Rafting of jack rabbit on kelp. Journal of Mammalogy
Pulquério MJF, Nichols RA. 2007. Dates from the molecular clock: How
wrong can we be? Trends in Ecology and Evolution 22: 180–184.
Raia P, Meiri S. 2006. The island rule in large mammals: Paleontology
meets ecology. Evolution 60: 1731–1742.
Raup DM. 1976. Species diversity in the Phanerozoic: An interpretation.
Paleobiology 2: 289–297.
Reed DH, O’Grady JJ, Brook BW, Ballou JD, Frankham R. 2003. Estimates of
minimum viable population sizes for vertebrates and factors inﬂuenc-
ing those estimates. Biological Conservation 113: 23–34.
Russell JC, Clout MN. 2005. Rodent incursions on New Zealand islands.
Pages 324–330 in Parkes J, Statham M, Edwards G, eds. Proceedings
of the 13th Australasian Vertebrate Pest Conference. Landcare
Sarnthein M, Bartoli G, Prange M, Schmittner A, Schneider B, Weinelt M,
Andersen N, Garbe-Schönberg D. 2009. Mid-Pliocene shifts in ocean
overturning circulation and the onset of Quaternary-style climates.
Climate of the Past 5: 269–283.
Severinghaus CW, Cheatum EL. 1956. Life and times of the white-tailed
deer. Pages 57–186 in Taylor WP, ed. The Deer of North America. Wild-
life Management Institute.
Simpson GG. 1940. Mammals and land bridges. Journal of the Washington
Academy of Sciences 30: 137–163.
Stankiewicz J, Thiart C, Masters JC, de Wit MJ. 2006. Did lemurs have
sweepstake tickets? An exploration of Simpson’s model for the colo-
nization of Madagascar by mammals. Journal of Biogeography 33:
Stephens PA, Sutherland WJ, Freckleton RP. 1999. What is the Allee effect?
Oikos 87: 185–190.
Terborgh J. 1974. Preservation of natural diversity: The problem of extinc-
tion prone species. BioScience 24: 715–722.
www.biosciencemag.org December 2013 / Vol. 63 No. 12 • BioScience 951
Thiede J. 1978. A glacial Mediterranean. Nature 276: 680–683.
Van den Hoek Ostende LW, Meijer HJM, van der Geer AAE. 2009. A bridge
too far. Comment on “Processes of island colonization by Oligo-
Miocene land mammals in the central Mediterranean: New data from
Scontrone (Abruzzo, Central Italy) and Gargano (Apulia, Southern
Italy)” by P. P. A. Mazza and M. Rustioni [Palaeogeography, Palaeo-
climatology, Palaeoecology 267 (2008) 208–215]. Palaeogeography,
Palaeoclimatology, Palaeoecology 279: 128–130.
Van der Geer A, Lyras G, de Vos J, Dermitzakis M[D]. 2010. Evolution of
Island Mammals: Adaptation and Extinction of Placental Mammals on
Van Duzer C. 2004. Floating Islands: A Global Bibliography. Cantor Press.
Van Valen LM. 1973. Pattern and the balance of nature. Evolutionary
Theory 1: 31–49.
Vigne J-D. Marinval-Vigne M-C. 1988. Contribution à la connaissance du
cerf de Corse (Cervus elaphus, Artiodactyla, Mammalia) et de son his-
toire. Bulletin d’Écologie 19: 177–187.
Wallace AR. 1869. The Malay Archipelago—The land of the orang-utan
and the bird of paradise: A narrative of travel with studies of man and
Warren BH, Strasberg D, Bruggeman JH, Prys-Jones RP, Thébaud C. 2010.
Why does the biota of the Madagascar region have such a strong Asiatic
ﬂavour? Cladistics 26: 526–538.
West JB. 2001. Snorkel breathing in the elephant explains the unique
anatomy of its pleura. Respiratory Physiology 126: 1–8.
Paul P. A. Mazza (paul.mazza@uniﬁ.it) is afﬁliated with the Department of
Earth Sciences at the University of Florence, Italy. Sandro Lovari is afﬁliated
with the Department of Life Sciences at the University of Siena, Italy. Federico
Masini is afﬁliated with the Department of Earth and Sea Sciences at the
University of Palermo, Italy. Marco Masseti is afﬁliated with the Leo Pardi
Department of Evolutionary Biology at the University of Florence. Marco
Rustioni is afﬁliated with the Museum of Paleontology in Montevarchi, Italy.