Durvillaeales

''Durvillaea'' is a genus of large brown algae in the monotypic family Durvillaeaceae. All members of the genus are found in the southern hemisphere, including Australia, New Zealand, South America, and various subantarctic islands. ''Durvillaea'', commonly known as southern bull kelps, occur on rocky, wave-exposed shorelines and provide a habitat for numerous intertidal organisms. Many species exhibit a honeycomb-like structure in their fronds that provides buoyancy, which allows individuals detached from substrates to raft alive at sea, permitting dispersal for hundreds of days over thousands of kilometres. ''Durvillaea'' species have been used for clothing, tools and as a food source by many indigenous cultures throughout the South Pacific, and they continue to play a prominent role in Chilean cuisine.

Common name and etymology

The common name for ''Durvillaea'' is southern bull kelp, although this is often shortened to bull kelp, which can generate confusion with the North Pacific kelp species ''Nereocystis luetkeana''.

The genus is named after French explorer Jules Dumont d'Urville (1790-1842).

Description

''Durvillaea'' species are characterised by their prolific growth and plastic morphology.

Two species, '' D. antarctica'' and '' D. poha'' are buoyant due to a honeycomb-like structure in the fronds of the kelp that holds air. When these species detach from the seabed, this buoyancy allows for individuals to drift for substantial distances, permitting long distance dispersal. In contrast, species as '' D. willana'' lack such 'honeycomb' tissue and are non-buoyant, preventing the individuals from moving long distances.

Ecology

''Durvillaea'' bull kelp grow within intertidal and shallow subtidal areas, typically on rocky wave-exposed coastal sites. '' D. antarctica'' and '' D. poha'' are intertidal, whereas '' D. willana'' is subtidal (to 6 m depths). Intertidal species can grow at the uppermost limit of the intertidal zone if there is sufficient wave wash. Species can withstand a high level of disturbance from wave action, although storms can remove individuals from substrates.

Epibionts, parasites and rafting

Holdfasts of '' D. antarctica'' and other species are often inhabited by a diverse array of epifaunal and infaunal invertebrates, many of which burrow into and graze on the kelp. In New Zealand, species that inhabit ''Durvillaea'' include the sea-star '' Anasterias suteri'', crustaceans such as '' Parawaldeckia kidderi'', '' P. karaka'', and the gribbles '' Limnoria segnis'' and '' L. stephenseni'', as well as the molluscs ''Cantharidus roseus'', ''Onchidella marginata'', ''Onithochiton neglectus'', and ''Sypharochiton sinclairi'', and the spider ''Desis marina''.Vink, C., McQuillan, B., Simpson, A., & Correa-Garhwal, S. (2017). The marine spider, ''Desis marina'' (Araneae: Desidae): new observations and localities. ''The Weta, 51'', 71-79. Retrieved from http://publications.ento.org.nz/index.php/weta/article/view/167

''Durvillaea'' individuals can detach from substrates, particularly during storms. Once detached, buoyant species such as '' D. antarctica'' and '' D. poha'' can float as rafts, and can travel vast distances at sea, driven by ocean currents. Specimens of ''D. antarctica'' have been found to float for up to 210 days, during which time high wind speeds transport kelp rafts up to 10,000 km. Environmental factors such as temperature, solar radiation and surface winds (all of which vary with latitude) affect buoyancy of southern bull kelp rafts and their rate of travel. Rafts of ''D. antarctica'' are more likely to disperse offshore if individuals detach during outgoing tides during autumn and winter. Rafts of Kelp-associated invertebrates can be transported inside of drifting kelp holdfasts, potentially leading to long-distance dispersal and a significant impact upon the population genetic structure of the invertebrate species.

Rafts of ''Durvillaea'' can be colonised by the goose barnacles ''Lepas australis'' and '' L. pectinata''. Beachcast, decomposing bull-kelp is colonised and consumed by a wide variety of invertebrates including sandhoppers ''Bellorchestia quoyana'', and kelp flies ''Chaetocoelopa littoralis''.

Other seaweeds including ''Gelidium lingulatum'', '' G. rex'', ''Corallina officinalis'' var. ''chilensis'', and ''Lessonia spicata'' also grow as epiphytes in the holdfasts of ''D. antarctica''. Rafting on ''D. antarctica'' appears to have influenced the dispersal and phylogeography of these non-buoyant species. In New Zealand, ''Durvillaea'' fronds can also be infected by the obligate red algal epiphyte ''Pyrophyllon subtumens'' (J. Agardh ex R.M. Laing) W.A. Nelson 2003.

Fronds of '' D. antarctica'' can be infected by an endophytic, phaeophycean algal parasite '' Herpodiscus durvillaeae'' (Lindauer) G.R. South. Fronds can also be infected ''Maullinia'', a genus of intracellular, protistan parasites. Based on genetic evidence, both ''H. durvillaeae'' and ''Maullinia'' have likely been dispersed across the Southern Hemisphere via rafting bull kelp.

Environmental stressors

Increased temperatures and heatwaves, increased sedimentation, and invasive species (such as ''Undaria pinnatifida'') are sources of physiological stress and disturbance for members of the genus.

A marine heatwave in the summer of 2017/18 appears to have caused the local extinction of multiple ''Durvillaea'' species at Pile Bay, on the Banks Peninsula. Once the kelp was extirpated, the invasive kelp ''Undaria pinnatifida'' recruited in high densities.

Disturbance from earthquake uplift

Earthquake uplift that raises the intertidal zone by as little as 1.5 metres can cause ''Durvillaea'' bull kelp to die off in large numbers. Increased sedimentation following landslides caused by earthquakes is also detrimental. Once an area is cleared of ''Durvillaea'' following an uplift event, the bull kelp that re-colonises the area can potentially originate from genetically distinct populations far outside the uplift zone, spread via long distance-dispersal.

Intertidal species of ''Durvillaea'' can be used to estimate earthquake uplift height, with comparable results to traditional methods such as lidar. However, since ''Durvillaea'' holdfasts often grow at the uppermost limit of the intertidal zone, these uplift estimates are slightly less accurate compared to measures derived from other intertidal kelp such as ''Carpophyllum maschalocarpum''.

Chile

The 2010 Chile earthquake caused significant coastal uplift (~0.2 to 3.1 m), particularly around the Gulf of Arauco, Santa María Island and the Bay of Concepción. This uplift caused large scale die offs of '' D. antarctica'' and dramatically affected the intertidal community. The damage to infrastructure and ecological disturbance caused by the earthquake was assessed to be particularly damaging for seaweed gatherers and cochayuyo harvest.

New Zealand

Akatore

''Duvillaea'' bull kelp diversity appears to have been affected by uplift along the Akatore fault zone. Phylogeographic analyses using mitochondrial COX1 sequence data and genotyping by sequencing data for thousands of anonymous nuclear loci, indicate that a historic uplift event (800 – 1400 years before present) along the fault zone and subsequent recolonisation, has left a lasting impact upon the genetic diversity of the intertidal species '' D. antarctica'' and '' D. poha'', but not on the subtidal species '' D. willana''. Such a genetic impact may support the founder takes all hypothesis. Further genetic analysis has revealed that the population structure of two epifaunal species, the gribble '' L. segnis'' and the chiton '' O. neglectus'', closely matches the pattern observed in the intertidal host species of ''Durvillaea'' along the Akatore fault zone. However, no matching pattern was observed for another epifaunal species, the amphipod '' P. karaka'', most likely because this species has better swimming potential and can rely upon other host seaweeds.

Kaikōura

A substantial die off of ''Durvillaea'' bull kelp occurred along the Kaikōura coastline following the 2016 Kaikōura earthquake, which caused uplift up to 6 metres. The loss of ''Durvillaea'' kelp caused ecological disturbance, significantly affecting the biodiversity of the local intertidal community. Aerial drone imaging two years after the earthquake indicated that ''Durvillaea'' abundance remained low on reefs with significant uplift, but it revealed offshore refuge populations less frequently detected by field researchers. Areas Genetic analysis indicated that some of the ''Durvillaea'' that subsequently reached the affected coastline (i.e. potential colonists) came from areas >1,200 kilometres away.

Wellington and the Wairarapa

Based on genetic data, the predominantly southern-restricted species '' D. poha'' appears to have undergone a recent range expansion into the North Island, as it can be found at low frequencies along the Wellington coastline. This range expansion coincides with areas affected by tectonic uplift and landslides caused by historic earthquakes, including the 1855 Wairarapa earthquake. The removal of ''D. antarctica'' and formation of new coastline by such tectonic disturbance likely provided an ecological opportunity for ''D. poha'' to successfully colonise coastline north of the Cook Strait.

A genetic study of '' D. antarctica'' identified distinct units of population structure across the uplift zone of the 1855 Wairarapa earthquake. Notably, two spatial-genomic sectors of ''D. antarctica'' were identified on Turakirae Head, which received the greatest degree of uplift (2 – 6 m). Phylogeographic modelling indicated that bull kelp that survived moderate uplift in the Wellington region (≤2 m) likely recolonised Turakirae Head via two parallel, eastward colonisation events - resulting in the two observed units of population structure. The hierarchical phylogeographic variation observed in the study provided non-experimental evidence of parapatric sectoring (see Founder takes all) as a result of natural disturbance, over a timescale observable to humans (i.e. <200 years).

It has been hypothesised that gaps in the current geographic range of '' D. willana'' around Wellington and the Wairarapa may have been caused by local extinction following historic earthquake uplift events such as the 1855 Wairarapa earthquake. However, uplift along the Akatore fault zone does not appear to have significantly affected the genetic diversity of ''D. willana'' in that region. The interpretation of this genetic result for Akatore was that earthquake uplift is likely insufficient to cause the complete extirpation of subtidal kelp species such as ''D. willana''.

Species and distribution

There are currently eight recognised species within the genus, and the type species is ''D. antarctica''.Bory de Saint-Vincent, J.B.G.M. (1826). Laminaire, ''Laminaria''. In: ''Dictionnaire Classique d'Histoire Naturelle''. (Audouin, I. ''et al.'' Eds) Vol. 9, pp. 187-194. All species are restricted to the Southern Hemisphere and many taxa are endemic to particular coastlines or subantarctic islands.

* ''Durvillaea amatheiae'' X.A. Weber, G.J. Edgar, S.C. Banks, J.M. Waters & C.I. Fraser, 2017,Weber, X.A., Edgar, G.J., Banks, S.C., Waters, J.M., and Fraser, C.I. "A morphological and phylogenetic investigation into divergence among sympatric Australian southern bull kelps (''Durvillaea potatorum'' and ''D. amatheiae'' sp. nov.)." Mol. Phylogenet. Evol. (2017) 107:630-643. endemic to southeast Australia.
* '' Durvillaea antarctica'' ( Chamisso) Hariot, found in New Zealand, Chile and various subantarctic islands including Macquarie Island.
* ''Durvillaea chathamensis'' C.H.Hay, 1979, endemic to the Chatham Islands.
* ''Durvillaea fenestrata'' C. Hay, 2019, endemic in the subantarctic Antipodes Islands.
* ''Durvillaea incurvata'' ( Suhr) Macaya, endemic to Chile.
* ''Durvillaea poha'' C.I. Fraser, H.G. Spencer & J.M. Waters, 2012, endemic to South Island of New Zealand, as well as the subantarctic Snares and Auckland Islands.
* ''Durvillaea potatorum'' ( Labillardière) Areschoug, endemic to southeast Australia.
* ''Durvillaea willana'' Lindauer, 1949, endemic to New Zealand.

Evolution

Time-calibrated phylogenetic trees using mixtures of mitochondrial and nuclear DNA markers have estimated that ''Durvillaea'' diverged from other brown algae approximately 20 to 60 million years ago. Given the modern distribution of extant ''Durvillaea'' species throughout the Southern Ocean, it has been suggested that the distribution may reflect vicariance following the break-up of Gondwana 40 to 50 million years ago, but this distribution can also be explained by the long-distance dispersal of buoyant ''Durvillaea'' lineages throughout the Southern Ocean. Based on molecular phylogenetic research, non-buoyancy is not necessarily the ancestral state for the genus, and non-buoyant lineages could have still been transported across the ocean when attached to rafts of different species of buoyant algae.

A phylogeny focused on the genus, based on four genes ( COI, rbcL, 28S and 18S) indicates the evolutionary relationships shown in the cladogram below. Notably, additional unclassified lineages were estimated within ''D. antarctica''. Mitochondrial introgression has been observed between two species, where some individuals with nuclear DNA of ''D. poha'' exhibited mitochondrial DNA belonging to ''D. antarctica''.

Use of ''Durvillaea'' species

Australia

'' D. potatorum'' was used extensively for clothing and tools by Aboriginal Tasmanians, with uses including material for shoes and bags to transport freshwater and food. Currently, ''D. potatorum'' is collected as beach wrack from King Island, where it is then dried as chips and sent to Scotland for phycocolloid