Hawaiian Drosophila

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Hawaiian Drosophila
Drosophila silvestris Kilohana 5161a.jpg
Drosophila silvestris
Scientific classification
Kingdom:
Animalia
Phylum:
Arthropoda
Class:
Insecta
Order:
Diptera
Family:
Drosophilidae
Subfamily:
Drosophilinae
Genus:
Drosophila
Subgenus:
Drosophila (subgenus)
Species groups
  • see text

The Hawaiian Drosophilidae are a lineage of flies within the genus Drosophila. This monophyletic clade includes all of the endemic Hawaiian Drosophila and all members of the genus Scaptomyza , which contains both Hawaiian and non-Hawaiian species. The Hawaiian Drosophilidae are descended from a common ancestor estimated to have lived 25 million years ago. [1] [2] Species of Hawaiian Drosophilidae flies have been studied as models of speciation and behavioral evolution. Along with other members of the native Hawaiian ecosystem, the conservations status of many species of Hawaiian Drosophilidae is threatened by habitat loss and introduced predators, among other factors. [3]

Contents

Diversity

There are an estimated 1,000 species of Hawaiian Drosophilidae. [1] As of 2022, 689 species have been described, including 273 species in the genus Scaptomyza , of which 148 are endemic to the Hawaiian archipelago, and 416 Hawaiian endemic species in the genus Drosophila. [4] Within the Hawaiian Drosophila there are several major groups, including the modified-mouthpart, modified-tarsus, and antopocerus species groups, and the picture-wing clade. [4]

Scaptomyza

The genus Scaptomyza , which contains both Hawaiian and non-Hawaiian species, is the sister lineage to the Hawaiian Drosophila, [2] and Hawaiian species in this genus are often included when speaking about the Hawaiian Drosophila generally. The Hawaiian and non-Hawaiian distribution of Scaptomyza can be explained as either the result of multiple colonizations of Hawaii, [5] or as the result of one colonization by the common ancestor of Scaptomyza and Hawaiian Drosophila, followed by several migrations back to continents. [6] [7] Scaptomyza is one of several genera that are currently nested within the genus Drosophila, rendering it paraphyletic. [1]

Hawaiian Drosophila

Picture-wing, nudidrosophila, ateledrosophila (PNA) clade

A picture-wing Hawaiian fly, Drosophila glabriapex Drosophila glabriapex.jpg
A picture-wing Hawaiian fly, Drosophila glabriapex

The picture-wing clade of Hawaiian Drosophila is named for the intricate patterns of melanin pigment on their wings. [8] This clade includes the grimshawi, planitibia, and adiastola species groups, among others.

Research on the taxonomy and biology of picture-wing flies in the 1970's led to the description of 105 species, with several more described in the decades since. [9] More recent studies on variation in wing patterns has led to the generation of a database devoted solely to wing diversity in the Hawaiian Drosophila lineage. [10] These flies have also been extensively studied for their courtship behavior, potential for hybridization between species, and larval ecology. [11] Many species of picture-wing flies breed in rotting bark and stems. [12]

Antopocerus, modified-tarsus, ciliated-tarsus (AMC) clade

The antopocerus species group includes 15 species of flies, notable for their large adult body size and egg size, as well as the prominent antennae on males. [13] Antopocerus was previously considered as a distinct genus, before being sunk into the genus Drosophila based on their phylogenetic position within other Hawaiian lineages. [14] Species of antopocerus flies have been described from the islands of Maui, Molokai, Lanai, Hawaii, and one species from Oahu.

The modified-tarsus species group is so named because of the variation in the shape and structure of front tarsi of males. [13] These tarsal modifications include flattened, spoon-shaped structures, elongated cilia, and clusters of bristles, and are thought to be used in mating displays. Antopocerus and modified-tarsus flies largely breed in rotting leaves.

Modified-mouthparts species group

The modified-mouthparts species group is named for the divergent forms of labellar structures relative to other Drosophila species. [15] This large group of flies has received relatively less study, in part due to their rarity and because many species are not attracted to typical Drosophila baits. These flies show a remarkable diversity in breeding ecology, with the majority of species using more than one host family for larval feeding. [12] There are more than 100 described species of modified-mouthparts flies, distributed throughout all major Hawaiian islands. [4]

Drosophila mimica, a modified-mouthparts species Drosophila mimica.jpg
Drosophila mimica , a modified-mouthparts species

Haleakalae species group

Haleakalae species are typically small, slender, and with shiny black bodies. [16] Rearing records indicate that members of this group breed exclusively on fungus. [12] There are more than 50 described species of Haleakalae flies, distributed throughout all major Hawaiian islands. [17] These species are characterized by their simple courtship displays, relative to some picture-wing species, and the short filaments on their eggs. Some species also have a black rim on the labellum.

Rustica species group

This enigmatic species group includes three species, described from Oahu, Molokai, and Hawaii, that been historically difficult to place within Hawaiian Drosophila because they display traits similar to multiple other groups. [18] These traits include a sclerotized rim on the labellum, reminiscent of several haleakalae species, and tarsi with cilia, reminiscent of ciliated-tarsus species in the AMC clade.

Research

Geographical distributions of Hawaiian Drosophila species and their host plants (e.g. Cyanea) have been studied to understand evolutionary radiations on islands. Hawaii speciation (Drosophila and Cyanea colonization).png
Geographical distributions of Hawaiian Drosophila species and their host plants (e.g. Cyanea ) have been studied to understand evolutionary radiations on islands.

Hawaiian Drosophila have been studied as models of speciation, population genetics and genomics, as well as for evolution of behavior and evolutionary development (aka evo-devo). [1] Research in the 1970s-80s by Hampton L. Carson and others studying patterns of chromosome banding, mating behavior, and hybridization helped resolve relationships between species and contributed to understanding of evolution on islands. [19] [20]

The genome of Drosophila grimshawi was selected to be one of the landmark 12 Drosophila genomes sequenced in 2007. [21] Since then the genome size of multiple species have been investigated, revealing genomic expansions in multiple lineages composed primarily of satellite DNA and noncoding sequences. [22]

Ecology and reproduction

Like many other members of the family Drosophilidae, Hawaiian species are largely saprophagous. [23] Female flies lay their eggs in a wide array of substrates, including rotting bark, leaves, fruit, sap, and fungi. Across species there is substantial diversity in the choice of host organism, using as many as 34 families of Hawaiian native flowering plants as hosts. [12] Many individual species are highly host specific and breed in only one substrate type from one or a few species.

Several groups of Hawaiian Drosophilidae show more unusual breeding habits for Drosophilidae flies, such as the cytrandrae species group (Scaptomyza cyrtandrae and S. neocyrtandrae), which breed on fresh Cytrandra leaves, and the Scaptomyza subgenus Titanochaeta, which breed in spider egg sacs. [12]

There is significant variation in reproductive morphology across species, including the number of ovarioles in the ovary, [24] the shape of the ovipositor, [25] and the size and shape of eggs. Research on the evolution of these traits suggests that variation is related to differences in the substrate where flies lay eggs. [23]

Status and conservation

Surveys of species abundance over time have shown a general decline in the number of Hawaiian Drosophilidae flies, along with other organisms in the native Hawaiian ecosystem. [3] Currently 13 species are listed as federally endangered: Drosophila aglaia , D. differens , D. digressa, [26] D. hemipeza , D. heteroneura , D. montgomeryi , D. musaphilia , D. neoclavisetae , D. obatai , D. ochrobasis , D. sharpi, [27] D. substenoptera , and D. tarphytrichia. One species, D. mulli , is listed as threatened. [3]

Threats to the conservation of Hawaiian Drosophilidae include loss-of-habitat, in part due to invasive pigs, goats, rats, deer, and cattle, as well as introduced predators such as big-headed ants, yellow crazy ants, and yellowjacket wasps. [3] In addition, invasive plants such as Psidium cattleianum , Lantana camara , Melinis minutiflora , and Rubus argutus can overwhelm native host plant species and outcompete them for access to sunlight. Flammable grass species such as Melinis minutiflora also contribute to rapidly spreading forest fires. These threats are especially relevant because many native host plants for Hawaiian Drosophilidae are already very rare.

Species groups

The following is a list of species groups contained within the Hawaiian Drosophilidae lineage: [2] [4]

Related Research Articles

<i>Drosophila</i> Genus of flies

Drosophila is a genus of flies, belonging to the family Drosophilidae, whose members are often called "small fruit flies" or pomace flies, vinegar flies, or wine flies, a reference to the characteristic of many species to linger around overripe or rotting fruit. They should not be confused with the Tephritidae, a related family, which are also called fruit flies ; tephritids feed primarily on unripe or ripe fruit, with many species being regarded as destructive agricultural pests, especially the Mediterranean fruit fly.

<span class="mw-page-title-main">Drosophilidae</span> Family of flies

The Drosophilidae are a diverse, cosmopolitan family of flies, which includes species called fruit flies, although they are more accurately referred to as vinegar or pomace flies. Another distantly related family of flies, Tephritidae, are true fruit flies because they are frugivorous, and include apple maggot flies and many pests. The best known species of the Drosophilidae is Drosophila melanogaster, within the genus Drosophila, also called the "fruit fly." Drosophila melanogaster is used extensively for studies concerning genetics, development, physiology, ecology and behaviour. Many fundamental biological mechanisms were discovered first in D. melanogaster. The fruit fly is mostly composed of post-mitotic cells, has a very short lifespan, and shows gradual aging. As in other species, temperature influences the life history of the animal. Several genes have been identified that can be manipulated to extend the lifespan of these insects. Additionally, Drosophila subobscura, also within the genus Drosophila, has been reputed as a model organism for evolutionary-biological studies, along with D. sechellia for the evolution of host specialization on the toxic noni fruit and Scaptomyza flava for the evolution of herbivory and specialist on toxic mustard leaves.

<span class="mw-page-title-main">Drosophilinae</span> Subfamily of flies

The Drosophilinae are the largest subfamily in the Drosophilidae. The other subfamily is the Steganinae.

<span class="mw-page-title-main">Sophophora</span> Subgenus of flies

The paraphyletic subgenus Sophophora of the genus Drosophila was first described by Alfred Sturtevant in 1939. It contains the best-known drosophilid species, Drosophila melanogaster. Sophophora translates as carrier (phora) of wisdom (sophos). The subgenus is paraphyletic because the genus Lordiphosa and the species Hirtodrosophila duncani are also placed within this subgenus.

<i>Zaprionus</i> Genus of flies

The genus Zaprionus belongs to the family fruit fly Drosophilidae and is positioned within the paraphyletic genus Drosophila. All species are easily recognized by the white longitudinal stripes across the head and thorax. The genus is subdivided in two subgenera, based on the presence of an even or odd number of white stripes. The species of the genus can be found in Africa and Southern Asia. One species, Zaprionus indianus, has invaded the New World.

<i>Scaptomyza flava</i> Species of fly

Scaptomyza flava is an herbivorous leaf mining fly species in the family Drosophilidae. In Latin, flava means golden or yellow. The fly is amber to dark brown in color and approximately 2.5 mm in length. In Europe and New Zealand the larvae are pests of plants in the order Brassicales, including arugula, brassicas, broccoli, Brussels sprouts, bok choy, cabbage, canola, cauliflower, horseradish, kale, kohlrabi, napa cabbage, nasturtium, radish, rapini, rutabaga, turnip, wasabi and watercress. In New Zealand, its range has expanded to include host species that are intercropped with salad brassicas, including gypsophila, otherwise known as baby's breath, which is in the pink family (Caryophyllaceae) and the pea in the Fabaceae. More typically, S. flava is oligophagous within the Brassicales. Scaptomyza are unusual within the Drospophilidae because the group includes species that are truly herbivorous. Other herbivorous drosophilids include D. suzukii, which attacks fruit very early during ripening and species within the genus Lordiphosa, from Africa and Asia, which also include leaf miners. Most drosophilids feed on microbes associated with decaying vegetation and sap fluxes.

<i>Scaptomyza</i> Genus of flies

Scaptomyza is a genus of vinegar flies, insects in the family Drosophilidae. As of 2022, there are 273 described species of Scaptomyza. Of those, 148 are endemic to the Hawaiian archipelago. This genus is part of the species-rich lineage of Hawaiian Drosophilidae, and is the sister lineage to the endemic Hawaiian Drosophila. The genus Scaptomyza is one of several nested within the paraphyletic genus Drosophila.

<span class="mw-page-title-main">Drosophila immigrans species group</span> Species group of the subgenus Drosophila

The Drosophila immigrans species group is a polyphyletic and speciose lineage of Drosophila flies, including over 100 species. Immigrans species belong to the Immigrans-tripunctata radiation of the subgenus Drosophila. Well-described species include Drosophila immigrans, and the sister species Drosophila albomicans and Drosophila nasuta. The genome of D. albomicans was sequenced in 2012 in an effort to characterize novel sex chromosome development in D. albomicans. Immigrans group species are related to mushroom-breeding Drosophila of the Quinaria and Testacea species groups.

<i>Drosophila silvestris</i> Species of fly

Drosophila silvestris is a large species of fly in the family Drosophilidae that are primarily black with yellow spots. As a rare species of fruit fly endemic to Hawaii, the fly often experiences reproductive isolation. Despite barriers in nature, D. silvestris is able to breed with D. heteroneura to create hybrid flies in the laboratory.

Drosophila acanthostoma is a species of fly in the genus Drosophila. It is found in Hawaii.

Drosophila aglaia is an endangered species of fly from Hawaii. This species is a member of the aglaia subgroup of the picture-wing clade of Hawaiian Drosophilidae. It is only found on the island of Oahu, and has not been observed since 1997, when it was found in Palikea.

Drosophila heteroneura is an endangered species of Hawaiian fly in the family Drosophilidae. This rare fly is part of the Hawaiian Drosophila lineage, and is only found in mesic and wet forests on the island of Hawaii.

Drosophila montgomeryi is an endangered species of fly from the lineage of Hawaiian Drosophilidae. It is found on the island of Oahu.

Drosophila tarphytrichia is an endangered species of fly from Hawaii, in the species rich lineage of Hawaiian Drosophilidae. It is only found on the island of Oahu. While originally collected near Manoa Falls in 1949, this fly is thought to have been extirpated from the Koʻolau Range and now only found in the Waiʻanae Range. This species is a member of the lanaiensis subgroup in the picture-wing clade.

Drosophila musaphilia is an endangered species of fly from Hawaii, in the species rich lineage of Hawaiian Drosophilidae. It is only found on the island of Kauai. The last reported sighting of this species was in 1988.

Drosophila obatai is an endangered species of fly from Hawaii, in the species rich lineage of Hawaiian Drosophilidae. It is only found on the island of Oahu. D. obatai is part of the orphnopeza subgroup in the picture-wing clade, and is closely related to D. sodomae, a fly found on the islands of Maui and Molokai.

Drosophila ochrobasis is an endangered species of fly from Hawaii, in the species rich lineage of Hawaiian Drosophilidae. It is found on the Big island of Hawaii, and has historically been recorded from four of the five volcanoes, though it is now largely absent from most of those sites. This species is in the adiastola subgroup and is closely related to D. setosimentum, but male D. ochrobasis have strikingly different wing markings.

Drosophila substenoptera is an endangered species of fly in the species rich lineage of Hawaiian Drosophilidae. It is only found on the island of Oahu,. Historically it was collected throughout the Ko'olau and Wai'anae ranges, but now is only known to occur near the summit of Mt. Kaala. D. substenoptera is a member of the planitibia species group and neopicta subgroup within the picture-wing clade.

Drosophila differens is an endangered species of Hawaiian fly in the family Drosophilidae. This species is a member of the planitiba subgroup of the picture-wing clade of Hawaiian Drosophila. It is found on the island of Molokai.

Drosophila digressa is an endangered species of fly from Hawaii, in the species-rich lineage of Hawaiian Drosophilidae. It is only found on the Big island of Hawaii. It was historically known from sites throughout the islands, but is now restricted to the Manuka and Ola'a reserves.

References

  1. 1 2 3 4 O'Grady, Patrick; DeSalle, Rob (2018). "Hawaiian Drosophila as an Evolutionary Model Clade: Days of Future Past". BioEssays. 40 (5): 1700246. doi:10.1002/bies.201700246. PMID   29603298. S2CID   4975629.
  2. 1 2 3 O'Grady, Patrick M.; Lapoint, Richard T.; Bonacum, James; Lasola, Jackline; Owen, Elaine; Wu, Yifei; DeSalle, Rob (2011). "Phylogenetic and ecological relationships of the Hawaiian Drosophila inferred by mitochondrial DNA analysis". Molecular Phylogenetics and Evolution. 58 (2): 244–256. doi:10.1016/j.ympev.2010.11.022. ISSN   1095-9513. PMID   21144904.
  3. 1 2 3 4 "Endangered and Threatened Wildlife and Plants; Determination of Status for 12 Species of Picture-Wing Flies From the Hawaiian Islands". Federal Register . Fish and Wildlife Service. June 8, 2006. pp. 26835–26852. Retrieved June 3, 2022.
  4. 1 2 3 4 5 6 Rampasso, Augusto Santos; O’grady, Patrick Michael (2022-03-08). "Distribution and Taxonomy of Endemic and Introduced Drosophilidae in Hawaii". Zootaxa. 5106 (1): 1–80. doi:10.11646/zootaxa.5106.1.1. ISSN   1175-5334. S2CID   247301097.
  5. ↑ Katoh, Toru; Izumitani, Hiroyuki F.; Yamashita, Shinji; Watada, Masayoshi (2017-02-10). "Multiple origins of Hawaiian drosophilids: Phylogeography of Scaptomyza Hardy (Diptera: Drosophilidae): Phylogeography of Scaptomyza". Entomological Science. 20 (1): 33–44. doi:10.1111/ens.12222. S2CID   88697632.
  6. ↑ O'Grady, Patrick; DeSalle, Rob (2008-04-23). "Out of Hawaii: the origin and biogeography of the genus Scaptomyza (Diptera: Drosophilidae)". Biology Letters. 4 (2): 195–199. doi:10.1098/rsbl.2007.0575. PMC   2429922 . PMID   18296276.
  7. ↑ Lapoint, Richard T.; O’Grady, Patrick M.; Whiteman, Noah K. (2013-10-01). "Diversification and dispersal of the Hawaiian Drosophilidae: The evolution of Scaptomyza". Molecular Phylogenetics and Evolution. 69 (1): 95–108. doi:10.1016/j.ympev.2013.04.032. ISSN   1055-7903. PMC   3769216 . PMID   23669011. S2CID   23700577.
  8. ↑ Eldon, Jon; Bellinger, M. Renee; Price, Donald K. (2019). "Hawaiian picture-winged Drosophila exhibit adaptive population divergence along a narrow climatic gradient on Hawaii Island". Ecology and Evolution. 9 (5): 2436–2448. doi:10.1002/ece3.4844. PMC   6405895 . PMID   30891191.
  9. ↑ Magnacca, Karl N.; Price, Donald K. (February 9, 2012). "New species of Hawaiian picture wing Drosophila (Diptera: Drosophilidae), with a key to species". Zootaxa. 3188 (1): 1–30. doi:10.11646/zootaxa.3188.1.1.
  10. ↑ Edwards, Kevin A.; Doescher, Linden T.; Kaneshiro, Kenneth Y.; Yamamoto, Daisuke (2007-05-30). "A database of wing diversity in the Hawaiian Drosophila". PLOS ONE. 2 (5): e487. Bibcode:2007PLoSO...2..487E. doi: 10.1371/journal.pone.0000487 . ISSN   1932-6203. PMC   1872047 . PMID   17534437.
  11. ↑ Magnacca, Karl N.; Price, Donald K. (2015-11-01). "Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae)". Molecular Phylogenetics and Evolution. 92: 226–242. doi:10.1016/j.ympev.2015.06.014. ISSN   1055-7903. PMID   26151218.
  12. 1 2 3 4 5 Magnacca, Karl N.; Foote, David; O’grady, Patrick M. (2008-03-17). "A review of the endemic Hawaiian Drosophilidae and their host plants". Zootaxa. 1728 (1): 1–58–1–58. doi: 10.11646/zootaxa.1728.1.1 . ISSN   1175-5334.
  13. 1 2 Lapoint, Richard T.; Magnacca, Karl N.; O’Grady, Patrick M. (2014-11-24). "Phylogenetics of the Antopocerus-Modified Tarsus Clade of Hawaiian Drosophila: Diversification across the Hawaiian Islands". PLOS ONE. 9 (11): e113227. doi: 10.1371/journal.pone.0113227 . ISSN   1932-6203. PMC   4242607 . PMID   25420017.
  14. ↑ Kaneshiro, Kenneth K. Y. (September 1976). "A revision of generic concepts in the biosystematics of Hawaiian Drosophilidae". Proceedings of the Hawaiian Entomological Society. 22: 255–278.
  15. ↑ Magnacca, Karl N.; O'Grady, Patrick M. (August 2009). Revision of the Modified Mouthparts Species Group of Hawaiian Drosophila (Diptera: Drosophilidae): The Ceratostoma, Freycinetiae, Semifuscata, and Setiger Subgroups, and Unplaced Species. ISBN   978-0-520-09873-2.
  16. ↑ Hardy, D. Elmo; Kaneshiro, Kenneth Y.; Val, Francisca Carolina do; O'Grady, Patrick M. (2001). "Review of the Haleakalae species group of Hawaiian Drosophila (Diptera: Drosophilidae)". Bishop Museum Bulletins in Entomology. 9: 1–88.
  17. ↑ O'grady, Patrick M. (2004). "Phylogenetic relationships within the Drosophila haleakalae species group inferred by molecular and morphological characters (Diptera: Drosophilidae)" (PDF). Bishop Museum Bulletins in Entomology. 12: 117–134.
  18. ↑ O'Grady, Patrick M.; Val, Francisca Carolina do; Hardy, D. Elmo & Kaneshiro, Kenneth Y. (2001). "The rustica species group of Hawaiian Drosophila (Diptera: Drosophilidae)". Pan-Pacific Entomologist. 77 (4): 254–260.
  19. ↑ Carson, Hampton L (1983-03-01). "Chromosomal sequences and interisland colonization in Hawaiian Drosophila". Genetics. 103 (3): 465–482. doi:10.1093/genetics/103.3.465. ISSN   1943-2631. PMC   1202034 . PMID   17246115.
  20. ↑ Kaneshiro, Kenneth Y. (1976). "Ethological Isolation and Phylogeny in the Planitibia Subgroup of Hawaiian Drosophila". Evolution. 30 (4): 740–745. doi:10.2307/2407814. ISSN   0014-3820. JSTOR   2407814. PMID   28563322.
  21. ↑ Drosophila 12 Genomes Consortium (2007). "Evolution of genes and genomes on the Drosophila phylogeny". Nature. 450 (7167): 203–218. Bibcode:2007Natur.450..203C. doi: 10.1038/nature06341 . ISSN   0028-0836. PMID   17994087.
  22. ↑ Craddock, Elysse M.; Gall, Joseph G.; Jonas, Mark (2016). "Hawaiian Drosophila genomes: size variation and evolutionary expansions". Genetica. 144 (1): 107–124. doi:10.1007/s10709-016-9882-5. ISSN   1573-6857. PMID   26790663. S2CID   14316335.
  23. 1 2 Kambysellis, Michael P.; Ho, Kin-Fan; Craddock, Elysse M.; Piano, Fabio; Parisi, Michael; Cohen, Jacob (1995-10-01). "Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny". Current Biology. 5 (10): 1129–1139. doi: 10.1016/S0960-9822(95)00229-6 . ISSN   0960-9822. PMID   8548285. S2CID   18280158.
  24. ↑ Kambysellis, M. P.; Heed, W. B. (1971). "Studies of Oogenesis in Natural Populations of Drosophilidae. I. Relation of Ovarian Development and Ecological Habitats of the Hawaiian Species". The American Naturalist. 105 (941): 31–49. doi:10.1086/282700. ISSN   0003-0147. JSTOR   2459386. S2CID   86670370.
  25. ↑ Craddock, Elysse M.; Kambysellis, Michael P.; Franchi, Lisa; Francisco, Peter; Grey, Marques; Hutchinson, Angela; Nanhoo, Shawn; Antar, Shyar (December 2018). "Ultrastructural variation and adaptive evolution of the ovipositor in the endemic Hawaiian Drosophilidae". Journal of Morphology. 279 (12): 1725–1752. doi:10.1002/jmor.20884. ISSN   0362-2525. PMID   30397938. S2CID   53224294.
  26. ↑ "Endangered and Threatened Wildlife and Plants; Determination of Endangered Species Status for 15 Species on Hawaii Island". Federal Register. Fish and Wildlife Service. November 29, 2013. pp. 64637–64690. Retrieved June 3, 2022.
  27. ↑ "Endangered and Threatened Wildlife and Plants; Determination of Endangered Status for 48 Species on Kauai and Designation of Critical Habitat". Federal Register. Fish and Wildlife Service. April 13, 2020. pp. 18959–19165. Retrieved June 3, 2022.
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