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A tale of three hotspots - the interplay of ecological and evolutionary processes in shaping arthropod communities of Sulawesi, Hawaii, and California

Abstract

Our planet is undergoing change at a rapid pace, with novel stressors including climate change, deforestation, and species invasion drastically altering ecosystems. Preservation of diverse biotic communities is vital toward the continued production of essential ecosystem services. However, developing effective management strategies is hindered by our limited knowledge of global biodiversity, the ways it was formed, and the ways it will respond to novel disturbance. My dissertation research begins to address these critical knowledge gaps using arthropod communities in three locations within biodiversity hotspots: Sulawesi, Hawaii, and California.

The first part of my dissertation focused on mountains across the island of Sulawesi, which is situated within the biodiversity hotspot of Wallacea. This region is known for its highly endemic fauna with affinities to both Asian and Australian taxa as well as its complex patterns of diversity structured into areas of endemism (AOEs). Despite its status as a biodiversity hotspot, there is a paucity of information for many taxonomic groups and particularly for arthropods, including order Araneae (the spiders). In my first chapter, titled “Using a COI mini-barcode to document novel spider diversity in the biodiversity hotspot of Wallacea”, I employed a new methodology to expedite sample processing and increase species documentation in spiders. Through sequencing 2,263 spiders, I discovered a remarkably diverse spider fauna, identifying 514 operational taxonomic units (OTUs). Additionally, I detected high turnover across elevational gradients and between mountains as well as evidence of lineages related to both Asian and Australian taxa.

The results of my first chapter guided my second chapter, titled “Patterns of colonization and in-situ diversification of the tetragnathid spiders in Sulawesi, Indonesia”. In this chapter, I explored diversification dynamics in this highly dispersive and diverse family. Using a multi-locus data set and the software BEAST, I estimated divergence times to investigate the evolutionary history of tetragnathids in Sulawesi. Consistent with the results from the mini-barcode data, the family Tetragnathidae was very speciose, with 42 putative species belonging to five genera (Tetragnatha, Dolichognatha, Leucauge, Tylorida and Mesida). The genera Mesida and Tylorida displayed the highest diversity, with 20 and 11 putative species respectively. Each genus had lowland clades across each mountain with deep divergence dates corresponding to the formation of Sulawesi. The mid-elevation zones on each mountain were predominantly filled by more recent colonizers rather than descendants from lowland taxa. Mesida was the sole genus found at the highest elevations. Despite their dispersive capabilities, the high elevations were not colonized by tetragnathids pre-adapted to high elevation but rather by diverged mid-elevation Mesida taxa.

In my third chapter, “The relative importance of stochastic and deterministic processes in the assemblage of leaf litter arthropod communities across an elevation gradient”, I aimed to expand my research to a community-level perspective of biodiversity formation. I used metabarcoding techniques to sequence non-spider arthropod leaf litter communities across the elevation gradient of one mountain (Gunung Dako), focusing on the interactions between stochastic and deterministic processes in community assembly. By employing tests of phylogenetic dispersion and a null model analysis, I found evidence for heterogenous selection being important in shaping both the low- and high-elevation communities. In contrast, mid-elevation communities were exclusively shaped by stochastic processes, possibly reflecting communities in an equilibrium-like state. Two of the higher elevation sites showed phylogenetic over-dispersion, often associated with competitive exclusion dynamics. Contrasting this, the most disturbed lowland site showed a significant pattern of phylogenetic under-dispersion that may indicate a strong environmental filter. This observation suggests that habitat conversion could exert a cost on lowland native taxa, instead favoring closely related taxa that have ecological strategies suitable for disturbed habitats.

Anthropogenic stressors pose a significant threat on arthropod communities, and I delved into two additional critical aspects of this issue. In my fourth chapter, titled “Invasion by an ecosystem engineer changes biotic interactions between native and non-native taxa”, I examined the effects of a plant invasion on biotic interactions. I did this by sequencing the gut content of an endemic spider, Pagiopalus spp., in both native forest and invaded habitat, analyzing changes in dietary composition between spiders. The results revealed that spiders from the invaded habitat were eating a less consistent diet with a higher proportion of non-native taxa. Furthermore, I observed a significant increase in parasite load, particularly entomopathogenic fungi, in the spiders from invaded habitat. These findings underscore the profound shifts in biotic interactions that occur following invasion, potentially imposing fitness costs on native spiders and other species.

Another significant consequence of global change is the alteration of disturbance regimes, exemplified by California wildfires. While fires are natural disturbances in many ecosystems in California, factors such as climate change, fire suppression, and human ignition events are changing where and how fires burn. In my fifth chapter titled “The importance of habitat type and historical fire regimes in arthropod community response following large-scale wildfires”, I investigated how arthropod communities in different habitat types responded following the California lightening complex fires of 2020. The study revealed that habitat type is related to how arthropod communities respond after a fire event. Habitat types that historically experienced regular, cyclical fires exhibited a recovery trajectory that led to a similar community composition as unburned sites by the following spring season. However, scrub habitats, which historically experienced wildfires every 100-500 years, displayed a deviation from the community composition of unburned habitats, indicating a negative effect of wildfires on less fire-adapted habitats.

My dissertation research highlights the extent of biodiversity left to be discovered in hyper-diverse locations, the complex processes involved in biodiversity formation and community assembly, and the consequences of various anthropogenic stressors on arthropod communities across different systems. This research underscores the importance of biodiversity documentation efforts in threatened locations and the need to conduct biodiversity research in an ecological and evolutionary context. Such endeavors will enable us to develop effective strategies to safeguard biodiversity amidst an era of global change. It is imperative that we act swiftly and decisively to protect our planet's remarkable biodiversity for the benefit of present and future generations.

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