An algivorous sea slug as a novel sampling tool and its implications for algal diversity, herbivore ecology, and invasive species tracking

Wade, Rachael
Sherwood, Alison R.
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The Bryopsidales is a diverse order of green algae that includes important members of the marine environment as carbon and nutrient cyclers, ecological engineers, and substrate providers. Because of their unicellular, yet macroscopic construction, and often diminutive stature (some <2 cm at maturity), reliable morphological characters are rarely available for clear species delineation. These issues serve to confound their identification and even collection using traditional sampling methods. To address these challenges, the algivorous sacoglossan sea slug Plakobranchus cf. ianthobapsus Gould was used as a novel sampling tool for the detection and identification of bryopsidalean algae in the Hawaiian Islands. This sea slug feeds on siphonous green algae and sequesters their chloroplasts, effectively becoming photosynthetic itself. Using a sequestration preference study (Chp. 1), P. cf. ianthobapsus was found to preferentially sequester chloroplasts from diminutive siphonous species versus larger and more abundant species, most likely due to behavioral and/or physiological constraints. Molecular assessment using cloning (Chp. 1) and metabarcoding (Chp. 2) of their stolen chloroplasts, or “kleptoplasts,” demonstrated that P. cf. ianthobapsus sequesters chloroplasts from up to 23 algal species, several of which are putative new species or records to the Hawaiian Islands. Furthermore, kleptoplast metabarcode data supported little community dissimilarity among sites across the Main Hawaiian Islands (MHI). In contrast, a coral-dominated site had a significantly dissimilar community assemblage compared to algal-dominated sites, suggesting that this diminutive algal community is cryptic and widespread within algal-dominated environments. Additionally, these data confirmed Plakobranchus as the first herbivore of the invasive green alga Avrainvillea lacerata (=Avrainvillea amadelpha sensu Brostoff) in Hawai‘i and expanded its known range in the archipelago. While this research expanded our understanding of kleptoplast source diversity, it is difficult to discuss herbivore host selection limitations without a complete algal inventory. To better understand host selection by P. ianthobapsus and a more comprehensive assessment of algal community diversity, metabarcoding of epilithic turf algae was conducted, allowing a direct comparison of recovered P. cf. ianthobapsus kleptoplasts (Chps. 1 &2) and algal species available in its environments. These data also provide a fine scale assessment of Avrainvillea distributions, as previous data (Chp. 2) suggested that A. lacerata exhibits a cryptic and diminutive morphology. Thus, these data provide a bridge between the kleptoplast diversity studies (Chps. 1 & 2) and invasive species phylogenetic studies (Chps. 4 & 5). The algal community metabarcode data suggested that P. cf. ianthobapsus only uses ~23% of the siphonous green algal species available to it, implying that the slug has more specific host selection than previously thought. Further, these results suggested that there is a clear taxonomic delineation in host selection with abundant representation of taxa from across the order Bryopsidales as well as the siphonous green algal order Dasycladales. P. cf. ianthobapsus nearly exclusively utilizes species from the bryopsidalean suborder Halimedineae, the exception being the bryopsidinean taxon Codum edule. These data also provide evidence of three new populations of A. lacerata on the west coast of Maui – the first documented spread of the alga apart from the islands of Kaua‘i and O‘ahu. The siphonous green alga Avrainvillea lacerata exhibits high morphological plasticity in Hawai‘i, making its identification difficult. A phylogenetic reconstruction using two plastid loci and incorporating type specimen genetic data suggested that this species, which had previously been morphologically identified as A. amadelpha by Brostoff (1989), is in fact A. lacerata, a cosmopolitan species found throughout the Caribbean and Indo-Pacific. Further, these results suggested that the alga identified as A. amadelpha in the Mediterranean is not in fact that taxon, although its true identity remains elusive based on assessment of specimens collected near Libya and Tunisia. Assessment of populations across O‘ahu’s south shore suggested that A. lacerata has likely been introduced to the Main Hawaiian Islands at least twice with genotypic heterogeneity correlated with the east and west sides of the island. In addition to the morphological and molecular assessment of the Hawai‘i and Mediterranean invasive species of Avrainvillea, a second Avrainvillea species was discovered from two urbanized estuaries on the south shore of O‘ahu in 2014 and 2017, respectively. Morphological and molecular assessment of specimens representative of the two populations supported the alga’s identification as A. erecta (Chp. 4). The alga was recovered from 12-40 m depths and was growing among the seagrass Halophila decipiens, and the siphonous green algae Halimeda kanaloana and Udotea sp. Because of the populations’ locations near harbors and high boat traffic areas, it is possible that the alga was introduced via ballast water or anchor entanglement. It is also possible that the alga rafted from the west Pacific as tsunami debris following the 2011 Tohoku earthquake. Because of the invasive nature of A. lacerata in Hawai‘i, continued monitoring and management of A. erecta is essential to mitigating any negative effects of its introduction. Exploring this unique slug-algal relationship from both organisms’ perspectives allows a more comprehensive understanding of the marine environments and communities of which they are members. This system has broad implications for algal biodiversity, exploration of community assemblages, herbivore ecology, and invasive species management.
Systematic biology, Molecular biology, Plant sciences, Avrainvillea, Hawaii, kleptoplasty, metabarcode, phylogeny, Plakobranchus
221 pages
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