Apodera angatakere, angatakere (Brehm, 1928

Duckert, Clément, Blandenier, Quentin, McKeown, Michelle, Hohaia, Holden, Luketa, Stefan, Wilmshurst, Janet, Lara, Enrique & Mitchell, Edward A. D., 2021, Superficially described and ignored for 92 years, rediscovered and emended: Apodera angatakere (Amoebozoa: Arcellinida: Hyalospheniformes) is a new flagship testate amoeba taxon from Aotearoa (New Zealand), The Journal of Eukaryotic Microbiology (e 12867) 68 (6), pp. 1-13 : 8-10

Taxonomic status of Apodera angatakere

( Nebela penardi )

Apodera angatakere was first briefly reported as Nebela penardi in a publication focusing mostly on copepods ( Brehm, 1928). Only two drawings were shown ( Figure 2D ) and no indication of size or scale was provided. Brehm had sent a moss sample containing testate amoebae to Eugène Penard who described the finding as follows: “It is similar to Nebela vas Certes (now Apodera vas), but differs therefrom in that the shell possesses a broad, hollow, and characteristic keel, which is always present and might well be regarded as a sufficient character to distinguish a new species. Ihave not been able to identify it with any known species.” ( Brehm, 1928). As a result, Brehm proposed to name the species Nebela penardi .

To our knowledge there is no further mention of this species in the scientific literature and the species has been overlooked since then. Notably, Deflandre did not mention it in his 1936 monograph of the genus Nebela ( Deflandre, 1936) . Moreover, at the time of its description, the name Nebela penardi Brehm, 1928 was preoccupied by Nebela penardi Heinis, 1914 . It is therefore a junior homonym of this species, which implies that Nebela penardi Brehm was unavailable and thus invalid.

As there is no known synonym for this taxon, we therefore rename it in agreement with ICZN article 60.3, and as we transfer it to a new genus both a new generic name and a new species epithet are required. Furthermore, as a side note, Heinis ( Heinis, 1914) used the name Nebela penardi to erroneously rename a taxon that, according to Deflandre (1936), corresponds to Nebela martiali (now Certesella martiali ). Nebela penardi Heinis is therefore a junior synonym of Certesella martiali.

Avery similar species was described under the name Nebela kenyana by Didier Chardez from mountain lakes in Kenya at over 4000 m a.s.l. ( Chardez, 1982). This species has a similar size and overall morphology including a hollow keel surrounding the fundus of the test and a distinct neck with swollen sides. However, it lacks the characteristic constriction at the base of the neck which defines Apodera and, in that, it is more similar to genus Padaungiella .

Choice of a species name—an iterative process involving the Māori Language Commission

The choice of a name was an iterative process involving all authors in collaboration with Te Taura Whiri Ite Reo Māori. We aimed to find a species name that would be appropriate for the organism and ideally reflect the specific morphology which could be described in general words as a flattened gourd with a constriction at the base of the neck and a hollow “keel.” We also aimed to represent the Mauri (life force) of this unique species that was named by Māori for them as kaitiaki (guardian) of Aotearoa (New Zealand).

The options considered were:

1. An amoeba with a hard shell. According to the Reed Dictionary of Modern Māori, the word “amoeba” is translated as “pūora hurikē” and a “hard shell” is translated as “anga.” Combining the two with the word “whai” meaning “in possession of” leads to the name “Pūora hurikē whaianga.”

2. Considering that a shelled amoeba is analogous to a miniature snail, the second option was “A snail with a keellike shell.” Snail and keel being respectively translated as “ngata” and “takere,” this would then form “Ngata anga whaitakere.”

3. An amoeba with a keel-like hull: Pūora anga whaitakere.

4. An amoeba with a keel: Pūora whaitakere.

5. Ashell with a keel: Anga whaitakere.

The fifth option was chosen both for the way it sounded and the fact that the name would describe well the morphology of the amoeba. However, in a final discussion, Mr. Ngahiwi Apanui from the Māori Language Commission suggested that the “whai” could be dropped to shorten the name. The final chosen name was then «Angatakere», to be pronounced aeŋaetɑkɛrɛ (AN-GAH-TAH-KEH-REH).

Implications for biodiversity estimates and conservation

It is estimated that 10% of the New Zealand mainland was covered by wetlands before human arrival around 780 cal. Yr BP ( Ausseil et al., 2011; McGlone, 2009), and while testate amoebae were too small to be recognized by Māori until the introduction of the microscope, the wetland habitats that supported these organisms were highly valued by Māori for centuries, as mahinga kai/hauanga kai (food gathering areas), rongoā (gathering plants for medicinal use) and for material resources. Wetland extent was minimally affected by early Māori settlers, although extensive deforestation of dryland forest by burning transformed the landscape ( Argiriadis et al., 2018; McWethy et al., 2010; Perry et al., 2014). Wetland loss rapidly accelerated after European arrival in the 1800s, largely for agricultural development, and is now only 10% of the original extent ( Ausseil et al., 2011). It is estimated that the 250,000 ha of wetlands that remain are under increasing pressure from drainage, area loss, fragmentation, grazing, fire, pollution, and climate change ( Meyer et al., 2013; Robertson et al., 2019). The fact that we can still find novel diversity or diversity that has been very poorly described in such habitats makes them even more precious and worthier of conservation.

Describing the still mostly unknown diversity of protists requires a major effort in basic taxonomy ( Heger et al., 2014). The magnitude of land-use changes and natural habitat destruction occurring throughout the world and the now well-established existence of restricted geographical distribution patterns in free-living protists ( Foissner, 2008) implies that a large proportion of protist diversity will likely disappear before it can be described, and thus the conservation of protists should indeed be a priority ( Cotterill et al., 2008; Qin et al., 2016). Apodera angatakere is a highly conspicuous genus of testate amoeba and has to date only been found in New Zealand. Large species are more likely to have restricted geographical distribution as shown empirically for terrestrial and subaquatic testate amoebae in the southern temperate and Antarctic zones ( Wilkinson, 1994), at the global scale ( Wilkinson, 2001; Yang et al., 2010) and confirmed by an atmospheric circulation modeling study ( Wilkinson et al., 2012). Given its large size it is likely an endemic taxon and as such could represent the first documented microbial species for which New Zealand has a conservation responsibility at the global scale. Apodera angatakere could therefore be considered as a flagship species for microbial biogeography and conservation.

Todiscover, or not to discover: that is the question

Columbus thought he had discovered a new world hitherto unknown to Europeans. But it was later established that the Vikings had already made this discovery before him. And of course, the sheer notion of this major discovery disregarded the fact that native populations had already colonized the Americas millennia before Europeans were even able to conceive of the idea of sailing across the ocean.

This history is mirrored in the story of Apodera angatakere : Just like Columbus one of us (EM) thought he had discovered a new species only to be brought to the attention by another one of us (SL) that it had been previously described in a publication on microcrustaceans which had escaped the attention of previous researchers studying testate amoebae in New Zealand. But just as the Vikings did not establish a permanent settlement in America, Brehm's discovery was lost to science, or almost so.

The microbial world remains unknown for most of the people but charismatic groups such as testate amoebae are useful as messengers of the invisible dimension of nature's wonders and our impact on the biosphere. The fact that A. angatakere is known only from New Zealand and is restricted to ecosystems that have been almost entirely destroyed since European colonization is a perfect illustration of the fact that many species are being lost before we even have a chance to describe them.

Taxonomic actions

Taxonomic summary:

Amorphea Adl et al. 2021

Amoebozoa Lühe 1913, sensu Cavalier-Smith 1998

Tubulinea Smirnov et al. 2005

Elardia Kang et al. 2017

Arcellinida Kent 1880

Difflugina Meisterfeld 2002 , sensu Kosakyan et al., 2016

Hyalospheniformes Lahr et al., 2019

Hyalospheniidae (Schultze 1877) Kosakyan et Lara 2012

Apodera angatakere ( Brehm, 1928) Mitchell, Blandenier & Duckert 2021 1928 Nebela penardi Brehm

Icon: Brehm, 1928 Fig. 52

Description: Test composed of two clearly distinct parts, a subcircular, oval, or ellipsoidal, compressed posterior part (body) and a neck. The two parts separated by a deep constriction around the entire base of the neck. Sides of the neck straight to slightly concave with a bulge at the base in broad view. The margins of the neck sometimes compressed. Body almost circular. Dimensions based on 63 specimens: 53 individuals from Taranaki Maunga, North Island, four from the Old Ghost Road, South Island, and six from the Keppler Track, South Island: Length (min.– average–max.): 186–208–226 µm, width: 120–148–167 µm, pseudostome: 39–44–50 µm. Circa 80 µm in breadth.

Etymology: In the Māori language “angatakere” can be translated to “a keeled shell,” referring to the conspicuous keel present on the outline of the test.

Neotype: Brehm did not preserve any specimen, and the original type material is only represented by two simple drawings without indication of size. Because small variations in the morphology of the test can be used to distinguish closely related species, only high magnification microphotographs can be used to accurately represent a species and reliably distinguish it from taxa yet to be described ( Duckert et al., 2020; Kosakyan et al., 2016). For this reason, we designate the specimen in pictures Figure 2E as the neotype. As we were unable to find unfractured tests at the previous type locality (Margaret's tarn, Mt. Rolleston near Arthur's pass, New Zealand South Island) the neotype has been designated among a population from Taranaki Maunga, New Zealand's North Island. However, tests from the previous type locality and the ones from Taranaki Maunga were similar in all points. Apermanent slide has been deposited at the Natural History Museum of Neuchâtel (Switzerland) with the ID 95-1.

New type locality: Ahukawakawa swamp , along the Pouakai crossing trail, on the saddle between Taranaki Maunga and Pouakai Hut, New Zealand's North Island. Coord: −39.255058°, 174.043106°, Elevation: 921 m a.s.l.

Geographical distribution: Known from New Zealand North and South Islands and Auckland Island. Likely also Campbell and Chatham Islands. We did not find it in Macquarie Island where all Apodera specimens lacked the characteristic hollow keel.

Habitat: Sphagnum and brown mosses in peatlands and alpine wetlands in New Zealand's North and South Islands, mosses in low Metrosideros forest (Auckland Island).

Remarks: We did not succeed in obtaining DNA sequences from material collected from the previous type locality (Margaret's tarn, Mt. Rolleston near Arthur's pass, New Zealand South Island) and found only fractured test unfit to be designated as the neotype, we thus chose a specimen from Taranaki Maunga, New Zealand's North Island as the neotype. Given that 13 distinct molecular clades were recorded within Hyalosphenia papilio, a common but smaller species commonly found in Holarctic Sphagnum peatlands ( Heger et al., 2013; Singer et al., 2019), it is possible that several cryptic or pseudo-cryptic species exist within A. angatakere and that specimens from Margaret's tarn constitute a distinct species. If this were the case a new species would need to be described from Margaret's tarn, New Zealand South Island with its own type locality. The Auckland Island record is based only on microscopic observation (not illustrated) and is considered valid given the characteristic morphology. Nevertheless, it would need to be further confirmed by molecular data.

Three COI gene sequences of Apodera angatakere and Apodera vas (352–655 bp) were deposited in GenBank under the number MZ615186 – MZ615188 and MZ615189 – MZ615191 , respectively.

ZooBank registration number: urn:lsid:zoobank.org:act:921D8CE1-EF0F-4839-B264-97ED438B5694.

Figures

F I G U R E 2 Top half: Apodera angatakere n. gen. n. sp. (A–C, E and F), five specimens from Ahukawakawa swamp, Taranaki Maunga, New Zealand's North Island (sample EM-2540): (A–C) three barcoded individuals, (D) Brehm's original drawing of Apodera angatakere (described as Nebela penardi) from Margaret's Tarn, Arthur's Pass, New Zealand's South Island, (E and F), two individuals from sample EM-2540 (LM and SEM, respectively). E is the holotype. Note the presence of a ca. 10 µm wide keel. All specimens illustrated here as well as in Figures S2–S8 were used for morphometrical analyses (Figure 1). Scale bars (20, 50, or 100 µm) are shown for all specimen but were not provided in the original description. Bottom half: Apodera vas. (G) barcoded specimen from Macquarie Island (sample EM-2764), (H–J) three specimens from forest litter collected on the lower slopes of Taranaki Maunga, New Zealand's North Island (sample EM-2543). (H and I) Two barcoded specimen, (J) SEM of a third individual; note the absence of a keel. The codes of the barcoded specimens are the same as in the phylogenetic tree (Figure 3)