Introduction
Habitat fragmentation plays a fundamental role both in shaping
biological communities and in intraspecific diversification. As barriers
to migration increase, or as population sizes decrease, the risk of
overall extinction of a taxon increases (Hanski 1989, Hanski & Gilpin
1991, Reed 2004). Moreover, the isolating matrix itself may facilitate
colonization from outside the system, by species better able to survive
in the new conditions created (Cacabelos et al. 2022, Hobbs 2001).
However, in some situations, the isolation created by fragmentation can
lead to species undergoing local adaptation (White et al. 2022), and
potentially even speciation when fragments merge after longer time
periods (Flantua et al. 2019). The latter situation is a key premise in
the theory that much of the evolution and diversification of life has
been driven by the coevolution of species with their ever-changing
ecological communities (the mosaic theory of coevolution; Thompson
2005), and the concept of constantly changing (evolving) metacommunities
(Urban & Skelly 2006). However, because fragmentation changes the
diversity and composition of entire biological communities, establishing
very different selective regimes in the different fragments (Kuli-Révész
et al. 2021), there are multiple feedbacks that affect the interplay of
colonization and extinction versus adaptation and speciation (De Meester
et al. 2016). Only through study at the scale of entire communities can
we start to develop insights into the role of fragmentation in
restructuring local communities on one hand and differentiation on the
other (Leibold et al. 2022).
Such large-scale analyses have long been limited by the sheer taxonomic
diversity of studied communities. Recent developments in high throughput
DNA barcoding now allow for the rapid inventory of entire communities at
multiple levels, from taxonomic composition to intraspecific genetic
variation (Arribas et al. 2022). This opens up unprecedented
opportunities to study community assembly in response to environmental
differences and habitat isolation (Emerson et al. 2022). These
techniques have been particularly useful in the study of arthropods, the
most species-rich animal taxon. Though arthropods are compelling to
study because of their ecological diversity and their centrality to the
food web of most terrestrial ecosystems, their overwhelming taxonomic
diversity makes the manual classification of community samples
impractical and means that this taxon is particularly underdescribed
(Emerson et al. 2016).
The current study couples a unique natural fragmentation experiment on
the Hawaiian Islands with a novel bulk community metabarcoding approach
to infer how entire arthropod communities change across discrete spatial
scales in a fragmented landscape, both in terms of species composition
and intraspecific differentiation. The Hawaiian Islands are ideal for
examining the effects of isolation: The archipelago itself is the most
isolated in the world, which means that there were very few successful
colonists (Wagner and Funk 1995). Within the archipelago, each island is
isolated, with many of the endemic lineages showing a pattern of
progression that follows the geological chronology of the islands from
older to younger (Shaw & Gillespie 2016). Within an island, isolation
is created by separation of volcanoes and, over the most recent time
scales, new lava flows that can carve up the existing forests
(Vandergast and Gillespie 2004, Vandergast et al. 2004). In the latter
case, lava flows from volcanic eruptions lead to isolation of forest
fragments for extended time periods, with forest regrowth on lava
substrate taking anywhere from 300 to 3,000 years depending on the
abiotic environment (Drake & Mueller-Dombois 1993, Clarkson 1998). The
early history of each island has been characterized by perpetual cycles
of such dramatic fragmentation (Carson et al. 1990). The effects of
these cycles can be observed in real time on the youngest island of
Hawaiʻi, where lava from active volcanoes has led to multiple episodes
of forest fragmentation. This pattern is striking on the slopes of Mauna
Loa Volcano, where flows have repeatedly covered the landscape over the
last 400,000 years, creating a patchwork of habitats in different
successional stages (Carson 1995). Here, mature forests have often been
surrounded by new flows, resulting in patches of forested “islands”
(kīpuka) of various sizes and distances from each other and from the
continuous forest. The contrast between forest and lava is stark, with
the forest patches being continuously wet and cool, while the
surrounding lava is dry and hot during the day and cold at night.
Hawaiian forest arthropods are well known for their narrow climatic
niches (Hiller et al. 2019, Lim et al. 2022) and hence expected to be
strongly isolated by the inhospitable lava (Vandergast et al. 2004,
Vandergast & Gillespie 2004).
A particularly well-studied kīpuka system is located along the
northwestern slopes of Mauna Loa, where a volcanic eruption in 1855 has
left a network of multiple forest patches separated by barren lava.
Studies in this location have provided evidence that kīpuka differ in
community composition (Knowlton et al. 2017, Mueller 2015), and that
arthropods that are specialized for the wet forest are largely isolated
in a kīpuka, with the isolation sufficient to allow populations in
different kīpuka to demonstrate genetic differentiation (Carson & Sato
1969, Vandergast et al. 2004).
It has long been speculated that a kīpuka-like landscape dynamic,
fostering repeated isolation events, may serve as a “crucible of
evolution” (Carson 1990). According to this hypothesis, the isolation
of populations by lava flows has played a key role in fueling adaptive
radiation on the Hawaiian Islands. At the same time, it provides a
natural experiment for testing how fragmentation affects the species
composition of habitat patches of different size and isolation; not only
are kīpuka sometimes very small, so unlikely to sustain a high diversity
of forest-specialists over time. This can be exacerbated by a
substantial “edge” of low native species diversity that penetrates an
estimated 20 m-deep into kīpuka forest (Vandergast & Gillespie 2004).
The declines in species diversity towards kīpuka edges and with
declining kīpuka size can make these fragments more prone to
colonization from non-indigenous species (Mueller 2015).
Here, we use the Mauna Loa kīpuka system to examine how entire
communities of arthropods have responded to habitat fragmentation over a
170 year period. We use a vegetation beating protocol (Lim et al. 2022)
to sample forest undergrowth arthropod communities at the core and edge
of 13 kīpuka of varying sizes and distances to each other. As a
comparison to the kīpuka, we sampled two transects in continuous forests
on the eastern and western slopes of Mauna Loa. We applied a
semiquantitative metabarcoding protocol, which allowed us to study
communities from the scale of taxonomic diversity to the scale of
intraspecific genetic differentiation. We hypothesize that
1) Due to the pronounced climatic specialization of Hawaiian forest
arthropods, lava will have presented a strong barrier to their
dispersal, resulting in a community-wide species-area effect.
Specifically, we expect smaller kīpuka to have lower taxonomic and
genetic diversity. We expect to see higher community turnover over
similar distances between kīpuka than between continuous forest sites.
For the same reason, species that are limited to the forest core of a
kīpuka will, on average, show more evidence for genetic differentiation
than species sampled across similar distances in continuous forest.
2) Given the environmental differences between forest at the core of the
kīpuka compared to the edges (Vandergast & Gillespie 2004), we expect
markedly different arthropod species composition between them. In
individual kīpuka, we expect forest-specialized taxa to dominate core
habitats. Meanwhile, we expect that fewer forest species will persist in
kīpuka edges, and that both edge habitats and adjacent lava matrix will
have been colonized by higher proportions of non-native taxa than kīpuka
cores or native forest habitats. Consequently, kīpuka should host
distinct communities in their cores versus their edges, excepting in the
case of the smallest kīpuka, which may behave almost entirely as edges.
3) The species-area effect of reduced species diversity with decreasing
kīpuka size should provide less biotic resistance, resulting in an
inverse relationship between kīpuka size and the proportion of
non-native taxa detected in both core and edge habitats.