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Caves are considered buffered environments in terms of their ability to sustain near-constant microclimatic conditions. However, cave entrance environments are expected to respond rapidly to changing conditions on the surface. Our study documents an assemblage of endemic arthropods that have persisted in Rapa Nui caves, despite a catastrophic ecological shift, overgrazing, and surface ecosystems dominated by invasive species. We discovered eight previously unknown endemic species now restricted to caves—a large contribution to the island's natural history, given its severely depauperate native fauna. Two additional species, identified from a small number of South Pacific islands, probably arrived with early Polynesian colonizers. All of these animals are considered disturbance relicts—species whose distributions are now limited to areas that experienced minimal historical human disturbance. Extinction debts and the interaction of global climate change and invasive species are likely to present an uncertain future for these endemic cavernicoles.
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doi:10.1093/biosci/biu090 Advance Access publication 2 July 2014
Disturbance Relicts in a Rapidly
Changing World: The Rapa Nui
(Easter Island) Factor
J. JUDSON WYNNE, ERNEST C. BERNARD, FRANCIS G. HOWARTH, STEFAN SOMMER, FELIPE N. SOTO-ADAMES,
STEFANO TAITI, EDWARD L. MOCKFORD, MARK HORROCKS, LÁZARO PAKARATI, AND VICTORIA PAKARATI-HOTUS
Caves are considered buffered environments in terms of their ability to sustain near-constant microclimatic conditions. However, cave entrance
environments are expected to respond rapidly to changing conditions on the surface. Our study documents an assemblage of endemic arthropods
that have persisted in Rapa Nui caves, despite a catastrophic ecological shift, overgrazing, and surface ecosystems dominated by invasive species.
We discovered eight previously unknown endemic species now restricted to caves—a large contribution to the island’s natural history, given
its severely depauperate native fauna. Two additional species, identified from a small number of South Pacific islands, probably arrived with
early Polynesian colonizers. All of these animals are considered disturbance relicts—species whose distributions are now limited to areas that
experienced minimal historical human disturbance. Extinction debts and the interaction of global climate change and invasive species are likely
to present an uncertain future for these endemic cavernicoles.
Keywords: caves, disturbance relict hypothesis, ecological shifts, fern–moss gardens, endemic species
Today, virtually no place on Earth exists that has
not been affected in some way by human activity.
Although caves may be considered somewhat buffered sys-
tems (in particular, the deepest reaches of caves), the subterra-
nean realm is no exception. Cave ecosystems are inextricably
linked to surface processes. Deforestation (Trajano 2000,
Ferreira and Horta 2001, Stone and Howarth 2007), inten-
sive agriculture (van Beynen and Townsend 2005, Stone and
Howarth 2007, Harley et al. 2011), livestock grazing (Stone
and Howarth 2007), invasive species introductions (Elliott
1992, Reeves 1999, Taylor etal. 2003, Howarth etal. 2007),
and global climate change (Chevaldonné and Lejeune 2003)
have all been documented to affect cave biology.
Subterranean ecosystems often support unique, species-
rich communities, including narrow-range endemic animals
restricted to the cave environment. In some regions, caves
have been identified as hotspots of endemism and subterra-
nean biodiversity (Culver etal. 2000, Culver and Sket 2002,
Eberhard et al. 2005). In addition, cave-restricted animals
are often endemic to a single cave, watershed, or region
(Reddell 1994, Culver et al. 2000, Christman et al. 2005)
and are frequently characterized by low population numbers
(Mitchell 1970). Consequently, many cave-restricted animal
populations are considered imperiled (Reddell 1994, Culver
etal. 2000).
How these animals colonized and ultimately became
restricted to caves is generally explained by one of two
hypotheses. Occurring primarily within the deepest, most
buffered portions of caves, troglomorphic (or cave-adapted)
animals are believed to be restricted to this environment
because of either climatic or adaptive shifts. The climatic
relict hypothesis suggests that, as surface conditions changed
(e.g., changes driving advances and retreats of glaciers), some
species survived in more-favorable conditions underground
(Jeannel 1943, Barr 1968). The surface-dwelling populations
ultimately went extinct, whereas the populations successfully
colonizing the hypogean environment persisted and evolved
into troglomorphic forms. As our knowledge of cave biology
improved in tropical regions, numerous troglomorphic spe-
cies were discovered where climatic shifts associated with
glaciations were less pronounced. Because this region was
never glaciated and was more climatically stable, tropical
cave-adapted animals did not fit the climatic relict paradigm.
On discovering epigean congeners living parapatrically with
their troglomorphic sister species, Howarth (1982) proposed
the adaptive shift hypothesis to explain this phenomenon.
He provided additional support for the hypothesis with the
observation that, in exposed cavernous rock strata, a sig-
nificant amount of organic material sinks into cave environ-
ments. Because caves are unsuitable habitats for most surface
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animals, only those animals preadapted to the subterranean
realm are able to exploit this habitat, establish a reproducing
population underground, and ultimately make an adaptive
shift by evolving into cave-adapted forms.
Some animals may become restricted to caves as a result
of anthropogenic activities alone and, as the extent of human
impacts on cave ecosystems increases, another explanation is
necessary to explain the occurrence of human-induced cave
restriction. In addition, as the global human footprint becomes
more pronounced and the effects of habitat loss and anthropo-
genic climate change accelerate, we anticipate that more distur-
bance relict species are likely to be found within both habitat
fragments and relict habitats in caves and on the surface, as
well. We propose the disturbance relict hypothesis to explain
the occurrence of once-wide-ranging animals now restricted
to a particular environment because of human activity.
This hypothesis is applicable beyond caves, because epi-
gean examples of this phenomenon have already been docu-
mented. For example, a walking-stick insect, Dryococelus
australis, presumed to have been driven to extinction by
the unintentional introduction of rats (Rattus rattus), was
recently rediscovered on Ball’s Pyramid, an islet near Lord
Howe Island, Australia (Priddel etal. 2003). Once occurring
throughout Lord Howe Island, the only wild population of
these animals is now restricted to cliff-face habitats on Ball’s
Pyramid, which are too steep for rats to access. Steep cliff
faces on the Hawaiian Islands are also known to support
endemic relict plant species, which have been extirpated
elsewhere on the islands through competition with nonna-
tive invasive plant species and predation by invasive pigs and
goats (Wood 2012). Of these, Wood (2012) reported range
rediscoveries of two cliff-face relicts and the possible recent
extinction of three cliff-face relicts. The presumed extinction
of these three plant species underscores the precarious per-
sistence of many relict populations as a result of mounting
anthropogenic pressures.
A case study from Rapa Nui caves
Famous for its megalithic statuary (moai), Rapa Nui (Easter
Island) has served as a cautionary parable for contempo-
rary societies of the perils of unsustainable resource use
(Diamond 2005). Several environmental and geographic
variables, including geographic isolation, a small size, a
shallow topographic relief, a low latitude relative to the equa-
tor, and aridity (when compared with other South Pacific
islands) predisposed Rapa Nui to dramatic human-induced
environmental change (Rolett and Diamond 2004). The
severity of human impacts was probably also exacerbated
by the sensitivity of the native ecosystem to fire (Mann
et al. 2008) and an extended drought during the time this
megalithic civilization emerged (e.g., Orliac and Orliac 1998,
Mann etal. 2008, Sáez etal. 2009, Stenseth and Voje 2009).
Because of the fragile environment and intensive human
demands placed on it, Rapa Nui appears to have experienced
a catastrophic ecological shift (sensu Scheffer etal. 2001) as
a result of large-scale deforestation soon after Polynesian
colonization, which occurred sometime between 800 and
1200 CE (Martinsson-Wallin and Crockford 2001, Hunt
and Lipo 2006, Wilmshurst etal. 2011). Evidence suggests
that during this time, the predominantly native ecosystem
shifted from a palm-dominated forest to a largely grassland
community (Flenley etal. 1991, Mann etal. 2008, Sáez etal.
2009).
Hundreds of years later, during the midnineteenth century,
Rapa Nui was converted into pastureland for a century-long
sheep-grazing operation (Fischer 2005). On the basis of a
fossil pollen analysis, Mann and colleagues (2008) found
evidence that a remnant population of the endemic palm
(Paschalococos disperta) may have persisted in rugged terrain
(perhaps the first documented disturbance relict), but the tree
was probably driven to extinction by livestock. Another once
island-wide endemic tree, the toromiro (Sophora toromiro),
lingered until the mid-1950s (Heyerdahl and Ferdon 1961)
but later became extinct in the wild (Flenley etal. 1991)—
another possible casualty of livestock grazing.
Today, the island environment is dramatically different
from what the first Polynesian colonists encountered. All
native terrestrial vertebrates and many native plants have
gone extinct. On the basis of fieldwork and the available
literature, JJW and FGH determined that nearly 400 arthro-
pod species are known to occur on Rapa Nui. Prior to this
current study, roughly 5% (21species) were believed to be
endemic (i.e., species believed to have evolved only on the
island) or indigenous (i.e., species that arrived and estab-
lished a population on the island without human assistance).
Of these 21 recognized endemic arthropods, only one
recently described species (Collembola: Coecobrya kennethi)
was detected within a cave (Jordana and Baquero 2008).
This discovery raised the question of whether additional
endemic arthropods use the subterranean environment. We
began a series of studies in 2008 to address this question. We
systematically surveyed arthropod communities in 10 Rapa
Nui caves and their adjacent surface habitats to find any
additional endemics and to determine the degree to which
they were restricted to cave habitats (refer to the supplemen-
tal material for our methods).
The Rapa Nui caves within our study area appear to exhibit
little environmental variation. We found that the average
temperatures range from 16.5degrees Celsius (°C; standard
deviation [SD]= 0.5°C) in entrances and skylights (n= 3
caves, hourly data collected over 4days in July and August
2008 and July and August 2009) to 19.4°C (SD=1.5°C) in
the deepest reaches of the caves (n= 4 caves, hourly data col-
lected over 4days in July and August 2011). We also found
that the cave atmospheric relative humidity maintained a
nearly water-saturated level in the deepest portions of the
caves studied during the sampling period, and we suspect
that these conditions persist during much of the year.
Although caves have been described as buffered environ-
ments (Tuttle and Stevenson 1978), environments within
the shallow reaches of caves are expected to be less resistant
to changing atmospheric conditions at the surface, whereas
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the deeper reaches of caves may be more insulated from the
surface environment. On Rapa Nui, the fern–moss garden
environment occurring within both cave entrances and
the areas beneath skylights (figure1) appears to have been
at least somewhat insulated from intensive environmental
changes that occurred on the surface. This habitat occurs
on the cave floors and low walls and extends from the light
zones (entrance area) into the twilight zones. The pres-
ence of a cave-restricted endemic fern (Blechnum paschale;
DuBois etal. 2013) and an endemic moss species (Fissidens
pascuanus; Ireland and Bellolio 2002) already suggests that
these partially protected environments represent an impor-
tant refugium on Rapa Nui.
Discovery of new endemic species in a severely
degraded landscape
We report the persistence of at least eight island-endemic
and two Polynesia-endemic arthropod species on Rapa
Nui that appear restricted to cave environments (table 1,
figure2). This discovery amounts to nearly one-third of the
known endemic species on the island. None of these ani-
mals were detected in previous entomological studies (e.g.,
Fuentes 1914, Olalquiaga 1946, Kuschel 1963, Mockford
1972, Campos and Peña 1973), nor did we detect them
during our surface sampling effort. All 10 endemic species
were found in the fern–moss gardens near cave entrances
or beneath skylights, and most of these species ranged fur-
ther into the caves. Seven of these species ranged into what
we identified as the transition zone (totally dark passages
between the twilight zone and the more stable deep zone),
and six were detected within the presumed deep zone (cave
passages characterized as completely dark with relatively
stable temperatures, nearly water-saturated atmosphere, and
little to no airflow; see Howarth 1982).
Two of the species have also been reported from a limited
number of other Polynesian islands and may have arrived
with early Polynesians. The ancient Polynesian navigators
are well known for traveling from island to island with
canoe plants (Whistler 2009). They introduced these plants
across the South Pacific Islands for food, medicine, materi-
als for canoe building, and other purposes. A new species
of isopod (Styloniscus sp.) was recently discovered on both
Rapa Nui and Rapa Iti (3400kilometers [km] to the south-
west of Rapa Nui). On Rapa Iti, this animal was collected
from the dead leaves of the bird’s nest fern (Asplenium
nidus). In addition, a springtail (Lepidocyrtus olena) previ-
ously known only on the Hawaiian Islands (Christiansen
and Bellinger 1992; 7224km to the north by northwest of
Rapa Nui) was also among the species found within Rapa
Nui caves. On Rapa Nui, we found both animals in cave
entrances within a forested pit entrance and in the fern–
moss gardens, as well as in the deeper reaches of several
caves. We suggest that these animals may represent canoe
bugs—arthropods transported across the South Pacific
Ocean aboard canoes within the soils of cultivars. We fur-
ther predict that these animals will be detected on interven-
ing islands in Polynesia.
Alternatively, these animals may have arrived by raft-
ing on vegetation debris. De Queiroz (2005) convinc-
ingly argued that the extent of global oceanic dispersal of
plants and animals has been underestimated. Therefore, we
wanted to examine this possibility for these two species. An
examination of a map of oceanic currents (USASF 1943)
suggests that dispersal between Hawaii and Rapa Nui is
unlikely, given three bands of dominating equatorial cur-
rents running in an oscillatory pattern easterly and westerly.
Therefore, it is unlikely that rafting debris carrying dispers-
ing animals could travel orthogonal to these prevailing
cross currents and ultimately reach the shores of Rapa Nui.
However, oceanic dispersal from Rapa Iti to Rapa Nui is
plausible, because the South Pacific Gyre spirals from Rapa
Iti toward Rapa Nui. Dispersal by rafting in the opposite
direction is unlikely.
None of the animals found during our study have mor-
phological characters suggestive of cave adaptation, nor
do we suggest that these animals retreated into caves in
Figure 1. Relict fern–moss garden habitats from two
different entrances of cave Q15-038, in Rapa Nui
National Park, on Easter Island, Chile. The endemic
fern (Blechnum paschale) occurs along cave floors and
walls amid several moss species. Most of the disturbance
relict species discovered were detected within this habitat.
Photographs: Dan Ruby, University of Nevada, Reno.
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Table 1. Endemic disturbance relict species identified from Rapa Nui National Park, Easter Island, Chile.
Class or
subclass Order Family
Genus and
species Location Endemism Endemism justification
Malacostraca Isopoda Philosciidae Hawaiioscia sp. Fern–moss
gardens, transition
zone
Rapa Nui
endemic Endemic genus previously
known only from four
species in lava tube
caves in Hawaii (Taiti and
Howarth 1997); differs
in presence of pigment
and well-developed
eyes
Malacostraca Isopoda Styloniscidae aStyloniscus sp. Fern–moss
gardens, transition
zone, forested pit
Polynesia
endemic Known only on Rapa Iti
and Rapa Nui; group of
species characterized by a
large lobe on the ischium
(second leg segment
proximal to the body)
on the seventh or last
pereopod (leg) of
the male
Collembola Entomobryomorpha Entomobryidae Coecobrya sp. Fern–moss
gardens, transition
zone, deep zone
Rapa Nui
endemic Distinct from Coecobrya
kennethi
Collembola Entomobryomorpha Entomobryidae C. kennethi Fern–moss
gardens, deep
zone
Rapa Nui
endemic Jordana and Baquero
2008; Rafael Jordana,
University of Navarra,
Pamplona, Spain,
personal communication,
29 August 2013
Collembola Entomobryomorpha Entomobryidae Entomobrya sp. Fern–moss
gardens, forested
pit
Rapa Nui
endemic Resembles Entomobrya
pseudodecora from Bahia
Blanca province, Brazil,
but differs in pattern on
fourth abdominal
segment and foot claw
characters
Collembola Entomobryomorpha Entomobryidae bLepidocyrtus
olena
Fern–moss
gardens, transition
zone, deep zone,
forested pit
Polynesia
endemic Known previously only on
Hawaii (Christiansen and
Bellinger 1992); slight
difference in distal
pleural seta of the
head may suggest
divergence from the
Hawaiian group
Collembola Entomobryomorpha Entomobryidae Pseudosinella sp. Fern–moss
gardens Rapa Nui
endemic Specimen does not match
any known Pseudosinella
species
Collembola Entomobryomorpha Entomobryidae Seira sp. Fern–moss
gardens Rapa Nui
endemic Has similar pattern to
Seira gobalezai, from
Hawaii, but the chaetotaxy
differs; also resembles
Seira reichenspergeri,
from Santa Catarina
province, Brazil, but foot
claw characters are
different
Collembola Entomobryomorpha Paronellidae Cyphoderus sp. Fern–moss
gardens, transition
zone
Rapa Nui
endemic A single specimen but
distinct from all other
Cyphoderus spp. in
combinations of many
characters
Insecta Psocoptera Lepidopsocidae Cyptophania
pakaratii
Fern–moss
gardens, deep
zone
Rapa Nui
endemic Sexually reproduces (all
other known Cyptophania
are parthenogenetic);
spermathecal sac
much larger and less
wrinkled than those
of other congeners
(Mockford and Wynne
2013)
Note: The transition zone is the aphotic zone between the twilight and cave deep zones (refer to Howarth 1982). The transition and deep zone
environments were estimated. aStyloniscus sp. was also detected within the leaf litter of ferns on Rapa Iti. bThis is the first record of this
springtail occurring off Hawaii.
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response to environmental change on the surface. Rather, as
the island-wide ecological shift to a grassland community
occurred, we suggest that these arthropods were already
using caves, as well as terrestrial surface habitats, just as
many of their close relatives do today. As suitable leaf-litter
and soil habitats became progressively unavailable because
of grassland expansion and intensive livestock grazing, these
animals were ultimately isolated and restricted to the cave
environment. Therefore, we believe that they represent a
previously common component of the predisturbance leaf-
litter and edaphic fauna. These species represent disturbance
relicts of animal populations that were historically more
broadly ranging.
In other regions of the globe, caves have been identified
as supporting relict species believed to have formerly ranged
widely in surface environments but that are now restricted
to the cave environment as a result of climatic shifts. In
the Western United States, moss gardens within some cave
entrances have been identified as relict habitats of the last
glacial maximum and now support species restricted to
these habitats (e.g., Benedict 1979, Northup and Welbourn
1997). Former leaf-litter-dwelling animals are also believed
to have retreated into caves and appear to be cave restricted
(rather than cave adapted) within all or a portion of their
former range because of the climatic shifts associated with
retreating and advancing glaciers (e.g., Peck and Lewis 1978,
Peck 1980, Shear etal. 2009).
Given the lack of glacial activity and the island’s long
history of intensive human use and disturbance, animals
now restricted to the cave environment on Rapa Nui are
more likely to represent human-induced disturbance relicts
than climatic relicts. As anthropogenic activities on Rapa
Nui continued (and perhaps accelerated), the wider ranges
(potentially island wide) that these animals once used dwin-
dled, and subpopulations ultimately became restricted to
pockets of suitable habitat (e.g., fern–moss gardens of caves).
Today, these disturbance relicts appear to be restricted only
to caves supporting these habitats.
Persistence uncertain for disturbance relicts on
Rapa Nui
Because most of the new species reported here are endemic
to Rapa Nui, we know that they have successfully endured
dramatic environmental changes and biological invasions
over the past several hundred years. However, half of these
endemics were detected in low numbers (i.e., n ≤ 5 indi-
viduals), and some of these animals may represent at-risk
populations. Extinction is often characterized by time lags,
and at-risk populations may persist for long periods of
time near extinction thresholds prior to becoming extinct
(Brooks et al. 1999, Hanski and Ovaskainen 2002, Vellend
etal. 2006). These extinction debts (see Tilman etal. 1994)
are often associated with populations that have been isolated
following a significant environmental perturbation, such
as habitat loss or fragmentation, as is the case with the dis-
turbance relicts presented here. In addition, none of these
species were found in surface habitats, and many of their
populations may be small. Therefore, recolonization of the
cave environment is probably very limited or nonexistent,
and the rescue effect (see Brown and Kodric-Brown 1977) is
unlikely to play a role in the long-term persistence for any of
these relict populations.
These animals have survived anthropogenic impacts
associated with a several-hundred-year history of intensive
human use, including deforestation, agriculture, and live-
stock grazing, as well as at least 100years of interactions (i.e.,
competition and predation) with invasive species. However,
even if extinction debt is not in play for these disturbance
relicts, these animals face an uncertain future because of
the associated impacts of global climate change, potential
competition with well-established invasive species, and fur-
ther competition with and predation by newly introduced
invasive species. Other researchers suggest that the interac-
tion of global climate change and invasive species presents
significant challenges for the persistence of surface-dwell-
ing endemic arthropods within other island ecosystems
(Vitousek etal. 1997, Chown etal. 2007, Fordham and Brook
2010), and we have found that these pressures are mounting
in Rapa Nui caves, as well.
We suggest that the combined effects of anthropogenic
climate change and competition, predation, and niche
Figure 2. Disturbance relict species in Rapa Nui caves.
(a)Hawaiioscia sp. (9.8millimeters [mm] long).
Micrograph: Caitlin Chapman and Neil Cobb, Colorado
Plateau Museum of Arthropod Biodiversity (CPMAB),
Northern Arizona University. (b)Styloniscus sp.
(3.2mm). Micrograph: Caitlin Chapman and Neil Cobb,
CPMAB. (c)Cyptophania pakaratii (2.8 mm). Source:
Reprinted with permission from Mockford and Wynne
(2013), courtesy of Zootaxa. (d)Coecobrya sp. (1.4mm).
(e)Pseudosinella sp. (0.8mm). (f)Lepidocyrtus olena
(1.2mm). (g)Coecobrya kennethi (1.1mm). (h)Seira sp.
(1.8mm). Micrographs (d–h): Ernest C. Bernard.
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displacement by invasive species will be among the greatest
threats to the persistence of these cave-restricted animals.
In particular, we expect different zonal environments to
respond differently to anthropogenic climate change. The
temperatures within cave deep zones approximate the aver-
age annual surface temperature (Pflitsch and Piasecki 2003,
Wynne et al. 2008), whereas the environment within the
cave entrance represents a combination of both surface and
cave climatic regimes (Howarth 1982, 1987). On the basis of
this relationship, we suggest that cave climates (temperature
and relative humidity) within the entrance and midcave
zonal environments will respond more quickly to rising sur-
face temperatures and that cave deep zone climates will have
a lag response. We expect cave-obligate species’ populations
to respond similarly. Animal populations occurring within
cave entrances and midcave areas may respond more quickly
than will populations occurring within cave deep zones.
Using information from other regions and South Pacific
islands, we expect that current climate change patterns
will present additional challenges for these endemic spe-
cies through changes in precipitation patterns. In general,
precipitation is expected to decrease in warmer subtropical
regions (IPCC 2007). Chu and colleagues (2010) reported
that long-term trends in increased drought conditions were
projected for the Hawaiian Islands, and it seems reasonable
to suggest that increased drought conditions may also occur
on Rapa Nui. This may result in the loss of some fern–moss
gardens from some caves, a reduction in area of this environ-
ment in other caves, or seasonal persistence of fern–moss
gardens in still other caves. By extension, this will present
challenges for the persistence of the endemic arthropod
populations that inhabit this environment.
Currently, three well-established invasive species may
pose considerable risk to the persistence of several endemic
populations of cavernicoles on Rapa Nui. For example,
Porcellio scaber, a globally distributed invasive isopod, was
the most commonly detected arthropod in both surface pit-
fall traps (n= 4100) and within caves (n= 402). Although
we did not specifically investigate competition between
native and invasive arthropod species, the low number of
individuals detected for the two endemic isopod species
compared with the large number of P. s c ab e r could be a
result of interspecific competition. In addition, Howarth
and colleagues (2001) considered P. s ca b er to be one of the
most damaging alien arthropods in the native ecosystems
in Hawaii. Oxidus gracilis, a cosmopolitan millipede (n=
146), and Periplaneta americana, the American cockroach
(n= 79), were the second and third most abundant invasive
arthropods detected in our study. On the Hawaiian Islands,
Stone and Howarth (2007) identified both of these species
as threats to endemic cavernicolous arthropod popula-
tions. Given the substantial number of opportunities for
additional invasive species introductions (due to regular
and frequent tourist travel to the island and the island’s
reliance on mainland Chile for perishable goods), these
endemic species may face additional pressures because of
competition and predation from newly colonizing invasive
species.
Conversely, provided these endemic species are able to
persist despite the growing threats of global climate change
and invasive species, Rapa Nui fern–moss gardens and the
endemic species that they support may serve as important
source habitats for endemics colonizing deep zone habi-
tats. In New Mexico lava tube caves, moss garden habitats
have been identified as supporting arthropod populations
capable of colonizing cave deep zones and, perhaps, evolv-
ing into cave-adapted forms (Northup and Welbourn 1997).
Of the Rapa Nui endemics, six of eight were detected
beyond the fern–moss garden habitats in the cave deep
zone environment. Given that troglomorphic relatives are
widely documented for both Isopoda and Collembola, it
is not unreasonable to suggest that some of these animals
may establish populations within cave deep zones and may
ultimately evolve into cave-adapted forms. In fact, all four
known congeners of Hawaiioscia sp., the Rapa Nui endemic
isopod, are troglomorphic species known only from the
Hawaiian Islands (Taiti and Howarth 1997).
Conclusions
As the human footprint becomes more pronounced on our
planet, we can expect to find once-widespread plant and ani-
mal species becoming isolated disturbance relicts restricted
to fragments of suitable habitat. Unfortunately, although
some large plant species (i.e., trees) may persist in small
areas, we do not anticipate large-body terrestrial vertebrates
to become disturbance relicts in small habitat fragments,
at least not without heavy extinction debts (see Newmark
1987, 1995). Animal disturbance relicts will probably include
smaller-body animals, such as arthropods, and perhaps small
vertebrate species. Present and future disturbance relicts
may have high extinction debts, and global climate change
and invasive species will likely further challenge the persis-
tence of these relict populations.
For Rapa Nui, despite these severe and persistent anthro-
pogenic impacts, the disturbance relicts presented here
persist today. However, we know nothing about the life
histories and population dynamics of these animals, nor do
we know to what extent human-induced climate change and
biological invasions may ultimately affect these populations.
Given that most of these disturbance relicts were detected in
low numbers, we suggest that the presumed cave-restricted
species presented here are imperiled. In addition, we have
demonstrated the importance of caves as repositories for
endemic species; nearly one-third of the island’s presently
known endemic arthropod species occur within caves.
Accordingly, the conservation and management of caves
and the fern–moss garden habitat should be considered the
highest priority for protecting the island’s endemic fauna.
Appropriate management of the caves supporting these
animals should include obtaining information on their life
history, population structure, and habitat requirements, as
well as identifying potential competitors and predators of
at AIBS on August 15, 2014http://bioscience.oxfordjournals.org/Downloaded from
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http://bioscience.oxfordjournals.org August 2014 / Vol. 64 No. 8 BioScience 717
these disturbance relict species. This information is urgently
needed to help safeguard their persistence in a rapidly
changing world.
Acknowledgments
Much gratitude is extended to Ninoska Cuadros Hucke,
Susana Nahoe, and Erique Tucky of Parque Nacional Rapa
Nui and Consejo de Monumentos, Rapa Nui, for their
guidance and support of this research. Cristian Tambley,
Campo Alto Operaciones, and Sergio Rapu Sr. provided
logistical support. Jabier Les of the Sociedad de Ciencias
Espeleológicas and Andrzej Ciszewski of the Polish
Expedition team provided cave maps. Christina Colpitts,
Lynn Hicks, Bruce Higgins, Alicia Ika, Talina Konotchick,
Scott Nicolay, Knutt Petersen, Pete Polsgrove, Dan Ruby,
and Liz Ruther provided assistance with field research. This
project was partially funded by the Explorers Club and the
National Speleological Society.
Supplemental material
The supplemental material is available online at http://
bioscience.oxfordjournals.org/lookup/suppl/doi:10.1093/biosci/
biu090/-/DC1.
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Thesis
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The importance of understanding species extinctions and its consequences for ecosystems and human life has been getting increasing public attention. Nonetheless, regardless of how pressing the current biodiversity loss is, with rare exceptions, extinctions are actually not immediate. Rather, they happen many generations after the disturbance that caused them. This means that, at any point in time after a given disturbance, there is a number of extinctions that are expected to happen. This number is the extinction debt. As long as all the extinctions triggered by the disturbance have not happened, there is a debt to be paid. This delay in extinctions can be interpreted as a window of opportunity, when conservation measures can be implemented. In this thesis, I investigated the relative importance of ecological and evolutionary processes unfolding after different disturbances scenarios, to understand how this knowledge can be used to improve conservation practices aiming at controlling extinctions. In the Introduction (chapter 1), I present the concept of extinction debts and the complicating factors behind its understanding. Namely, I start by presenting i) the theoretical basis behind the definition of extinction debts, and how each theory informed different methodologies of study, ii) the complexity of understanding and predicting eco-evolutionary dynamics, and iii) the challenges to studying extinctions under a regime of widespread and varied disturbance of natural habitats. I start the main body of the thesis (chapter 2) by summarizing the current state of empirical, theoretical, and methodological research on extinction debts. In the last 10 years, extinction debts were detected all over the globe, for a variety of ecosystems and taxonomic groups. When estimated - a rare occurrence, since quantifying debts requires often unavailable data - the sizes of these debts range from 9 to 90\% of current species richness and they have been sustained for periods ranging from 5 to 570 yr. I identified two processes whose contributions to extinction debts have been studied more often, namely 1) life-history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Less studied are the microevolutionary dynamics happening during the payment of a debt, the delayed conjoint extinctions of interaction partners, and the extinction dynamics under different regimes of disturbances (e.g. habitat loss vs. climate change). Based on these observations, I proposed a roadmap for future research to focus on these less studies aspects. In chapters 3 and 4, I started to follow this roadmap. In chapter 3, I used a genomically-explicit, individual-based model of a plant community to study the microevolutionary processes happening after habitat loss and climate change, and potentially contributing to the settlement of a debt. I showed that population demographic recovery through trait adaptation, i.e. evolutionary rescue, is possible. In these cases, rather than directional selection, trait change involved increase in trait variation, which I interpreted as a sign of disruptive selection. Moreover, I disentangled evolutionary rescue from demographic rescue and show that the two types of rescue were equally important for community resistance, indicating that community re-assembly plays an important role in maintaining diversity following disturbance. The results demonstrated the importance of accounting for eco-evolutionary processes at the community level to understand and predict biodiversity change. Furthermore, they indicate that evolutionary rescue has a limited potential to avoid extinctions under scenarios of habitat loss and climate change. In chapter 4, I analysed the effects of habitat loss and disruption of pollination function on the extinction dynamics of plant communities. To do it, I used an individual, trait-based eco-evolutionary model (Extinction Dynamics Model, EDM) parameterized according to real-world species of calcareous grasslands. Specifically, I compared the effects of these disturbances on the magnitude of extinction debts and species extinction times, as well as how species functional traits affect species survival. I showed that the loss of habitat area generates higher number of immediate extinctions, but the loss of pollination generates higher extinction debt, as species take longer to go extinct. Moreover, reproductive traits (clonal ability, absence of selfing and insect pollination) were the traits that most influenced the occurrence of species extinction as payment of the debt. Thus, the disruption of pollination functions arose as a major factor in the creation of extinction debts. Thus, restoration policies should aim at monitoring the status of this and other ecological processes and functions in undisturbed systems, to inform its re-establishment in disturbed areas. Finally, I discuss the implications of these findings to i) the theoretical understanding of extinction debts, notably via the niche, coexistence, and metabolic theories, ii) the planning conservation measures, including communicating the very notion of extinction debts to improve understanding of the dimension of the current biodiversity crisis, and iii) future research, which must improve the understanding of the interplay between extinction cascades and extinction debts.
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SYNTHESIS OF PARTS 11-20 OF THE ADDITIONS AND CORRECTIONS TO LIENHARD & SMITHERS, 2002: "PSOCOPTERA (INSECTA) – WORLD CATALOGUE AND BIBLIOGRAPHY". Since the volume Psocoptera (Insecta) – World Catalogue and Bibliography was published by the Geneva Natural History Museum in 2002, twenty supplementary papers of additions and corrections have appeared in Psocid News. All available literature on Psocoptera was treated in the same style as the Catalogue (listed taxonomically, faunistically and thematically). For ease of use a synthesis of the first ten supplements was published as Special Issue 3 of Psocid News. The present compilation offers a synthesis of the supplements 11 to 20 (published annually between 2012 and 2021 in Psocid News No. 14-23) and it contains a complement to the Subject Bibliography published in Psocid News Special Issue 2, i. e. a synthesis of the annual subject bibliographies published in Psocid News No. 19-23. See: http://hdl.handle.net/2115/35519
Article
Changes in well-delimited Collembola communities along a steep microclimatic gradient at the entrance of Silická ľadnica Ice Cave, Slovakia, were investigated after 10 years (2007, 2017). We focused on the occurrence of psychrophilic and endemic species occupying this unique karst collapse doline and their response to climatic singularities in the given years as well as the increasing trend in regional air temperature. The soil temperature means at sites across the doline slope corresponded with climatic trends in the periods 2006-2007 and 2016-2017. Significantly lower average soil temperatures but significantly higher mean abundances, species richness, and diversity indices of the collembolan communities were recorded at sites during the second study period, which was characterized by more favorable soil microcli-matic conditions (temperature and moisture content) compared to the first period. The dominance structure and community composition of the studied assemblages appeared to be relatively constant after 10 years, indicating stable collembolan communities , especially at cold sites at the bottom of the doline. Redundancy ordination analysis documented a clear delimitation of the communities in relation to the soil temperature, pH, and C:N ratio in both periods. Long-term (30-year) regional climatic data showed an increasing trend of annual air temperature means and precipitation. However, an increase in the number and abundance of xerothermophilous species and a decline in psychrophilic species (mostly endemic) along the gradient as a potential response of the increasing regional temperature were not observed, suggesting the high resilience of these communities. Microclimate and habitat heterogeneity are probably major drivers of soil Collembola communities along the steep microclimatic gradient of a karst collapse doline, which was observed by the repeated sampling after 10 years. Karst dolines as potentially important local sources of ɑ-diversity will likely become increasingly indispensable refugia for local biodiversity under ongoing global warming, thus deserving reliable conservation. K E Y W O R D S ɑ-diversity, climate changes, endemicity, refugium, resilience
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Elton featured isolated islands as particularly devastated by invasions, focusing on Easter Island, the Tristan da Cunha group, the Hawaiian chain, and New Zealand. Had he completed a second edition, he would have noted even greater impacts at least for Tristan de Cunha and Hawaii, as he had notes from publications on invasion impacts there from 1959 through 1970.
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Sometime around 1000 B.C., a people who would eventually be known as the Polynesians ventured into the Pacific and established a homeland in Tonga on the western side of a huge expanse of ocean and scattered islands known as the Polynesian triangle. This triangle has its angles at Hawai‘i (north), Easter Island (east), and New Zealand (south). Over the next two millennia or so, these intrepid voyagers explored and settled nearly every inhabitable island in the region by means of outrigger or double-hulled canoes. Hence the poetic name for this maritime culture, the canoe people.” Living on a distant tropical South Pacific island is not as easy as it may seem. Protein food, such as fish and birds, would be easy to find (at least in the beginning), but native vegetables, starches, and fruits that provide the staff of life were virtually absent. Timber trees were usually abundant, but native plants needed for making clothing, shelter, cordage, medicine, and material goods were remarkably scarce in prehistoric Polynesia. To remedy this absence of plants essential to their culture, the Polynesians employed a strategy of transporting the plants they needed (called canoe plants, which are part of the “Polynesian toolkit”) with them in their voyaging canoes. Around 60 of these canoes plants were present in the first area of Polynesia settled (western Polynesia, i.e., Samoa and Tonga). But during the eastward expansion into eastern Polynesia (Tahiti, Hawai’i, the Cook Islands, etc.), many of these failed to make the trip. Only about 27 canoe plants were present in the northeastern-most corner of Polynesia, Hawai‘i, at the time of the arrival of Europeans into the area. These canoe plants, along with native species mostly used for timber, were essential to life on the distant islands. This book is about the useful plants of the Polynesians, but most of the same species are also a part of Micronesian and Melanesian culture. It is basically an ethnobotanical flora with profiles of the 96 plants most important to the Polynesians (including the Fijians). These species are listed in alphabetical order, each with one or more photos of the plant and its uses. Each profile includes the scientific name, plant family, common name (some do not have English names) and the Polynesian names, along with a discussion of the origin of these names. It is followed by a discussion of the plants’ origin, range, habitat, and frequency. The end of the profile includes a botanical description, with a “distinguishing features” line to help in identification if the photos are insufficient. A table is provided that shows the distribution of each of the species within the major islands and island groups of Polynesia (including Fiji). Also included are a bibliography of pertinent literature and a glossary of botanical terms. A future book planned by the author will explore their cultural uses in much greater detail. The 241-page book includes about 148 color photos, and eight color illustrations by well-known Hawai‘i artist Mary Grierson. The book is designed for use by botanists (especially ethnobotanists), naturalists, teachers, students, or just nature lovers who are interested in the traditional useful plants of the islands. Other related books written by the author and available include The Samoan Rainforest, Rainforest Trees of Samoa, The Ethnobotany of Samoa, Flowers of the Pacific Island Seashore, Samoan Herbal Medicine, Tongan Herbal Medicine, Polynesian Herbal Medicine, Tropical Ornamentals, and Wayside Plants of the Islands. https://www.amazon.com/Plants-Canoe-People-Ethnobotanical-Polynesia/dp/0915809001
Article
Of the 15 species found, all are terrestrial and 5 are probably now limited to stream caves in the canyon as troglobites or disjunct populations of troglophiles. These 5 species probably descended from forest litter-inhabiting ancestors living near the caves during past glacial-pluvial climates. This 'life zone' lowering occurred most recently from 24 000 to 14 000 yr ago. When the forest retreated upwards at the beginning of the present interglacial (about 8000 yr ago), some of the litter invertebrates which had entered the caves were locally isolated in them when adjacent epigean populations went extinct. -from Author
Chapter
This chapter discusses collembola or springtails which comprise one of the most widespread and abundant groups of terrestrial arthropods. Collembola have three thoracic segments and six or fewer abdominal segments, including a telson consisting of a dorsal and two ventral valves surrounding the anus. There are typically four antennal segments, each with musculature. Collembola vary enormously in form and somewhat in internal anatomy, but all lack malpighian tubules and most have paired labial nephridia that empty into the ventral groove at the base of the labium. One universal and unique feature is the ventral tube or collophore–—an istally weakly paired projection from the first abdominal segment with membranous diversity of form equal to that seen in any other order of insects. Collembola rarely interact overtly with humans. There are no parasitic Collembola and they are not known to transmit any disease. Collembola play an important role in the development and maintenance of healthy soils, but this is not generally appreciated.
Chapter
Obligatory cavernicoles, or troglobites, have traditionally been of special interest to evolutionary biologists for several reasons. The existence of animal life in caves and other subterranean spaces at first attracted attention because of its novelty; intensive biological exploration of caves began little more than a century ago. Although the discovery and description of the cave faunas of the world is far from complete, especially in the Western Hemisphere, so much descriptive information has been compiled that we can safely assert that, at least in unglaciated, temperate parts of the world, the occurrence of numerous species of troglobites in any major limestone region is a common and highly probable phenomenon.