Research Article |
Corresponding author: Gary L. Miller ( gary.miller@ars.usda.gov ) Academic editor: Roger Blackman
© 2014 Gary L. Miller, Andrew S. Jensen, Mark A. Metz, Robert R. Parmenter.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Miller G, Jensen A, Metz M, Parmenter R (2014) A new species of Atheroides Haliday (Hemiptera, Aphididae) native to North America. ZooKeys 452: 35-50. https://doi.org/10.3897/zookeys.452.8089
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We report and describe the first species of Atheroides Haliday presumed to be native to North America, collected at the Valles Caldera National Preserve, New Mexico, USA. We hypothesize its placement among the Siphini based on morphological, phylogenetic analysis and extend the distribution of the genus to the Holoarctic. We expand the key of the known Atheroides to include the new species and discuss the current hypotheses of the geographic distribution of the type species, Atheroides serrulatus Haliday.
Valles Caldera National Preserve, Nearctic, cladistics, new species, Atheroides , Aphididae , Chaitophorinae , Siphini
The Jemez Mountains in northern New Mexico, USA, constitute a “sky island” at the southern end of the Rocky Mountains of North America. This area now serves as a Pleistocene biological refugium, supporting high-elevation ecosystems left behind by the last retreating Ice Age 20,000 years ago (
Atheroides is part of the tribe Siphini Mordvilko, 1928, the most derived clade of the Chaitophorinae Mordvilko, 1909, and was treated extensively by
We follow the recommendations of
We made observations with both stereo and compound microscopes at magnifications from 100-400×. We used a Visionary Digital BK Lab System® and SolMate® Trans-Illumination System to take digital photographs of slide-mounted specimens with a Canon® EOS 5D Mark II DSLR camera. We montaged Z-stacks with Helicon Focus Pro®. Illustrations were first hand-drawn using a Nikon® Eclipse E600 and a drawing tube. Final illustrations were rendered on Denril® multi-media vellum using Pigma® Micron® 005 and 01 technical pens. We performed digital image editing/enhancement/manipulation in the Gnu Image Manipulation Program (GIMP). Dimensions of structures in the description are reported in millimetres; for apterous viviparae the first measure is that of the holotype and the second that of the paratype; for oviparae ranges are followed by means in parentheses.
We approached the phylogenetic analysis with the assumptions that Siphini was monophyletic and part of the Chaitophorinae, that the species in question was undescribed, and that the new species belonged to Siphini. The phylogenetic question was the correct generic placement of the new species. We sampled taxa within Siphini so as to have all of the type species of the currently included genera (
We stored the HT apterous adult female and two oviparous adults collected in Valles Caldera National Preserve in 95% ethanol at -20 °C, until the DNA extractions were performed. We extracted DNA non-destructively with Qiagen®’s Blood & Tissue kits (Valencia, CA) using a technique described by
We were able to resolve a total of 12 binary morphological characters to address the question of generic placement of the new species among the genera of Siphini. Description of characters and character states included in the analysis follow:
0. Ratio of the Entire Body Length to the Body Width Measured Side to Side Across the Siphunculi
0 Body length less than 3× width of body
1 Body length at least 3.5× width of body
1. Number of Antennal Segments
0 Six
1 Five
A five-segmented antenna has long been considered a diagnostic feature of Siphini among aphid workers and was corroborated by
2. Ratio of Length of Dorsad Apical Seta of Antennal Segment III to Width of Antennal Segment III Measured at Middle
0 Seta length at least 1.3× width of antennal segment 3 at middle
1 Seta absent or seta length subequal or less than width of antennal segment 3
The new species is notable among Siphini in having short, sparse setae on the antenna, particularly antennal segment III. We used a ratio of the length of the most apical dorsal seta on antennal segment III to the width of antennal segment III at the middle of the segment since that width did not vary considerably among the taxa investigated. The new species shares the derived state with A. serrulatus.
3. Ratio of the Length of the Processus Terminalis to the Base of the Terminal Antennal Segment
0 Processus terminalis shorter or subequal in length to the base of the terminal antennal segment
1 Processus terminalis at least 1.5× longer than the base of the terminal segment
The ratio of the lengths of the base of the terminal antennal segment and the processus terminalis is used extensively among aphid taxa for genus and species level identification. This character is stable among taxa in the analysis − autopomorphic for Chaetosiphella berlesei − so is uninformative in this tree hypothesis, but is left in for the benefit of future work in the group.
4. Ratio of Hindfemur Length to Midfemur Length
0 Hindfemur length less than 1.5× length of midfemur
1 Hindfemur length at least 1.6× length of midfemur
The new species is notable among Siphini in having a short femur on the fore- and midlegs, particularly as compared to the femur of the hindlegs. The new species shares the derived state with A. serrulatus.
5. Shape of the Setae on the Dorsum of the Body
0 Dorsal setae almost exclusively acuminate
1 Dorsal setae scale-like, denticulate, and/or flabellate
The new species shares with other species of Atheroides the presence of non-acuminate setae throughout the body surface. The setae of the dorsum are characteristic of this diagnostic feature. The new species shares the derived state with A. serrulatus.
6. Denticulate or Spiculate Cuticle Covering Most of Body
0 Absent
1 Present
The integument between setal sockets may have raised, densely-distributed extensions that can be acuminate or blunt, as opposed to smooth cuticle. The derived state of this character does not support any monophyletic group resolved in the tree hypothesis.
7. Dorsal Cuticular Surface Wrinkles and Folds
0 Absent
1 Present
The new species shares with other species of Atheroides the presence of wrinkles and/or folds throughout the dorsal cuticle of the body reminiscent of the surface of the human brain. The new species shares the derived state with A. serrulatus.
8. Position of the Base of the Siphunculi
0 On abominal segment VI
1 On abdominal segment V
The primitive state among Aphididae is for the siphunculi to be positioned on tergite VI. Among most Siphini the position of the siphunculi is on tergite V. The tree hypothesis created from this analysis suggests that the derived state supports the monophyly of Siphini sans Caricosipha paniculata with a reversal in Laingia psammae.
9. Orifice of Siphunculus
0 Elevated above the surface of the abdomen on a tube
1 Flush with the surface of the abdomen or on a short mound of cuticle, not elevated by a tube
The primitive state among Aphididae is for the siphunculous to be in the form of a tube or cylinder such that the external orifice is elevated above the surface of the dorsum. The new species shares the derived state with all the species of Siphini included in the analysis except Caricosipha paniculatae.
10. Posterior Margin of Tergite VIII
0 Not expanded posteriorly, cauda visible in dorsal view
1 Expanded posteriorly hiding cauda mostly or completely from dorsal view
The new species shares with the derived state with Atheroides serrulatus and Laingia psammae.
11. Shape of cauda
0 Constricted basally or subbasally creating an apical knob
1 Broadly rounded, truncate, or emarginate
The new species shares with other species of Atheroides the shape of the cauda, being broadly rounded, truncate, or emarginate as opposed to having a posterior elongation or a constriction with an apical knob. The new species shares the derived state with all the species of Siphini included in the analysis except Caricosipha paniculatae and the two species of Sipha (Sipha).
There were no missing or inapplicable characters in the matrix. The complete matrix is given in Table
Single, most parsimonious tree of 14 steps (CI=85, RI=88) resulting from an exhaustive search in TNT. Closed circles indicate unique forward changes. Open circles indicate either forward changes with homoplasy or reversals. Numbers on nodes in squares indicate Bremer support values for that node.
Character | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Taxon | 0 | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 |
Chaitophorus leucomelas Koch, 1854 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Sipha (Rungsia) elegans Del Guercio, 1905 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 1 | 0 | 1 |
Sipha (Rungsia) maydis Passerini, 1860 | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 1 | 0 | 1 |
Sipha (Sipha) flava (Forbes, 1885) | 0 | 1 | 0 | 0 | 0 | 0 | 1 | 0 | 1 | 1 | 0 | 0 |
Sipha (Sipha) glyceriae (Kaltenbach, 1843) | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 1 | 0 | 0 |
Caricosipha paniculatae Börner, 1939 | 0 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
Laingia psammae Theobald, 1922 | 1 | 1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 1 | 1 | 1 |
Chaetosiphella berlesei (Del Guercio, 1905) | 0 | 1 | 0 | 1 | 0 | 0 | 1 | 0 | 1 | 1 | 0 | 1 |
Atheroides vallescaldera sp. n. | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
Atheroides serrulatus Haliday, 1839 | 1 | 1 | 1 | 0 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 |
We amplified and sequenced a 652 bp DNA fragment containing the barcoding region of the mitochondrial COI gene from the HT and two oviparous vouchers. Since all individuals produced sequences that were identical, only one sequence was submitted to GenBank (accession number KJ737374). We searched for matching sequences in GenBank and found multiple matches for Aphididae, but there were no sequences available for the taxa sampled in the phylogenetic analysis with enough overlap to warrant inclusion.
Atheroides
Atheroides Haliday, 1839: 189. Type species Atheroides serrulatus Haliday, 1839: 189 by subsequent designation (
Apteroides Mordvilko, 1929: 91. (Subsequent misspelling)
Corealachnus Paik, 1971: 3. Type species Corealachnus suwonensis Paik, 1971: 4 by original designation.
This new species can be distinguished from other species in the genus by the following combination of characters: setae on the dorsum flabellate and dentate, and arranged in rows; dorsum sclerotized with rugose sculpturing; marginal setae of abdominal tergites I-VI easily visible, longer than width of hindfemur at middle, acuminate; empodial setae flat, but with base and apex of equal width, not spatulate.
(slide-mounted specimens). Apterous vivipara (Figs
Atheroides vallescaldera n. sp. 4 holotype habitus (Left side focal planes from dorsum to middle. Right side focal planes from middle to ventral surface.) 5 antenna of apterous vivipara 6 head (left half dorsal, right half ventral) 7 ultimate rostral segments 8 examples of dorsal abdominal setae variation 9 tergite VIII (dorsal) 10 empodial setae 11 anal and genital figs. (Scale indicated by 0.20 mm measure bars and corresponding figure number.).
Morphometric data for apterous viviparae and oviparae of Atheroides vallescaldera sp. n.
A. vallescaldera sp. n. |
A. serrulatus (from |
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---|---|---|---|---|
Oviparae | Viviparae | Oviparae | Viviparae | |
N=8 | N=2 | N=6 | N=17 | |
Body [mm] | 2.08–2.30 | 2.07–2.21 | 2.00–2.35 | 1.70–2.20 |
Antenna [mm] | 0.54–0.58 | 0.53–0.55 | - | - |
Antenna / Body [times] | 0.24–0.27 | 0.25–0.26 | 0.21 | 0.19 |
Ant. segm. III [mm] | 0.17–0.19 | 0.17–0.18 | - | - |
Ant. segm. IV [mm] | 0.06–0.08 | 0.07–0.07 | - | - |
Ant. segm. V base [mm] | 0.07–0.09 | 0.08–0.08 | - | - |
Ant. Segm. V base / Ant segm. III [times] | 0.41–0.53 | 0.44–0.49 | 0.50–0.55 | 0.50–0.70 |
Ant. segm. V processus terminalis [mm] | 0.07–0.09 | 0.08–0.08 | - | - |
Ant. segm. V processus terminalis / Ant. segm. III [times] | 0.39–0.53 | 0.43–0.45 | - | - |
Ant. segm. V processus terminalis / base [times] | 0.77–1.29 | 0.89–1.03 | 1.00–1.05 | 0.77–0.91 |
Ant. Segm. V / Ant. Segm. III [times] | 0.82–1.00 | 0.89–0.92 | 1.00–1.10 | 1.10–1.30 |
Ant. Segm. V / Ant. Segm. IV [times] | 2.07–2.58 | 2.27–2.33 | 3.00–3.25 | 2.20–3.50 |
Ultimate rostral segm. [mm] | 0.12–0.13 | 0.12–0.13 | 0.07–0.10 | 0.07–0.10 |
Ultimate rostral segm. / its basal width [times] | 1.77–2.36 | 2.10–2.15 | - | - |
Ultimate rostral segm. / Ant. segm. V base [times] | 1.43–1.79 | 1.50–1.53 | - | - |
Ultimate rostral segm. / Ant. segm. III [times] | 0.66–0.76 | 0.67–0.73 | 0.69 | 0.69 |
Ultimate rostral segm. / Hind tarsus, 2nd segm. [times] | 0.77–1.00 | 0.83-0.98 | 0.75 | 0.75 |
Hind femur [mm] | 0.33–0.38 | 0.37–0.37 | - | - |
Hind tibia [mm] | 0.55–0.65 | 0.62–0.62 | - | - |
Hind tibia / Body [times] | 0.26–0.29 | 0.28–0.30 | - | - |
Hind tarsus, 2nd segm. [mm] | 0.13–0.14 | 0.13–0.14 | - | - |
Siphunculus width [mm] | 0.02–0.03 | 0.02–0.03 | - | - |
DNA barcode (COI) for the holotype and one paratype contains 652 nucleotides (GenBank # KJ737374):
GAACTTTATATTTTTTATTTGGAATTTGATCAGGACTAATTGGTTCTTCACTAAGAATTTTAATTCGATTAGAATTAAGACAAATTAATTCAATCATTAATAATAATCAATTATATAATGTTATCATTACAATTCATGCATTTATTATAATTTTTTTTATAACTATACCAATTGTAATTGGTGGATTTGGAAATTGATTAATCCCTTTAATAATAGGATGCCCTGATATATCATTCCCACGATTAAATAATATTAGATTTTGAATACTTCCACCAGCATTAATATTTATAATTATAAGTTTTATAATTAATAATGGAACAGGAACAGGATGAACAATTTACCCCCCTCTATCTAACAATATTGCCCATAATAATATTTCTGTTGACTTAACAATTTTTTCTCTACATTTAGCAGGAATCTCATCAATTTTAGGAGCAATCAATTTTATTTGCACAATTATAAATATAATACCTAATAATATAAAAATTAATCAAATTCCTCTTTTCCCTTGATCTATTTTAATTACAGCAATCTTATTAATTTTATCTTTACCTGTATTAGCAGGTGCAATTACTATACTTTTAACTGATCGAAATCTTAATACTTCATTTTTTGATCCTTCAGGAGGTGGAGACCCTATCTTGTATCAACA
Alate vivipara and male: unknown.
Ovipara (n = 8): Dorsal abdominal setae on segments I-VII 0.015–0.070. With 18–27 circular pseudosensoria on each hindtibia predominantly organized in pairs that are 8-shaped, others are single circles or triplets (conjoined pairs or triplets are still counted as single pseudosensoria). Otherwise similar to apterous vivipara. Morphometric data are in Table
The specific epithet, vallescaldera, is derived from the locality in which the specimens were collected, the Valles Caldera National Preserve, and should be considered a compound noun in apposition.
Type-locality. USA: NEW MEXICO: Sandoval Co., near unit 12, lower Santa Rosa Creek watershed, a perennial stream tributary of the Rio San Antonio, 35.951; -106.521, VCNP# 144, 23.ix.2010, 2,595m, A. Jensen coll., ex grass in open meadow next to Santa Rosa Creek, dominated by sedges, grasses, rushes and a variety of forbs (Fig.
Holotype apterous vivipara (Figs
Original label: “New Mexico: Valles Caldera Nat’l Preserve Near Unit 12 22 Sept. 2010 ex: grass in open meadow A. Jensen coll. SEL VCNP#144 Balsam”
Paratypes: same data as holotype (1 apterous vivipara USNMENT 00826486, 8 oviparae USNMENT 00826487-89, USNMENT 00826480-84).
Unknown bunch grass. All other known Atheroides spp. feed on a variety of grasses (Poaceae), sedges (Cyperaceae) and rushes (Juncaceae) (
1 | Setae on the dorsum of the body exclusively acuminate | 2 |
1’ | Setae on the dorsum of the body acuminate, forked, dentate, and/or flabellate | 3 |
2 (1) | Spinal setae very long, as long as or longer than marginal ones. Cauda covered by abdominal tergite VIII. On Deschampsia caespitosa | doncasteri Ossiannilsson, 1955 |
2’ | Marginal setae very long, longer than spinal ones. Cauda not covered by abdominal tergite VIII. On various grasses | hirtellus Haliday, 1839 |
3 (2’) | Dorsum partially sclerotic without visible sculpture. Antennal segment III with 4–8 long setae. On Festuca ovina and Stipa splendens | karakumi Mordvilko, 1948 |
3’ | Dorsum sclerotic with visible, rugose sculpture. Antennal segment III with 0–4 short setae. On various grasses | 4 |
4 (3’) | Dorsal setae arranged in visible rows | 5 |
4’ | Dorsal setae not arranged in visible rows | 6 |
5 (4) | Marginal setae of abdominal tergites I–VI short, hardly visible, rarely as long as width of hindfemur, dentate. Empodial setae spatulate, flat and broadened at apex | serrulatus Haliday, 1839 |
5’ | Marginal setae of abdominal tergites I–VI easily visible, longer than width of hind femur at middle, acuminate (Fig. |
vallescaldera sp. n. |
6 (4’) | Body elongate, oval, 1.50–2.40 mm long. Antennae 4- or 5-segmented, 0.12–0.15 times body length. Antennal segment I with 2 pointed and 1 dentate seta | brevicornis Laing, 1920 |
6’ | Body elongate, slender, nearly linear, 1.55–1.72 mm long. Antennae 5 segmented, 0.18–0.25 times body length. Antennal segment I with 1 erect fan-shaped seta | persianus Wieczorek, 2009 |
1 | Hind tibiae with more than 30 pseudosensoria. Marginal setae of abdominal tergites I-VI short, hardly visible, rarely as long as width of hind femur, dentate. Empodial setae spatulate, flat and broadened at apex | serrulatus Haliday, 1839 |
1’ | Hind tibiae with less than 30 pseudosensoria. Marginal setae of abdominal tergites I-VI easily visible, longer than width of hindfemur at middle, acuminate (Fig. |
vallescaldera sp. n. |
We have shown that A. vallescaldera is morphologically most similar to A. serrulatus among described Atheroides, yet there are clear morphological differences between the species. The facts that it is found in such an unusual geological feature as the Valles Caldera, and far from the known populations of A. serrulatus in Canada, suggest that A. vallescaldera is native to North America. This is a simpler explanation than the notion that two species of Atheroides have invaded North America, with one being unknown in the Palearctic yet establishing in an isolated and unique habitat in North America. Further, we suggest that it is possible that A. serrulatus is naturally Holarctic as opposed to adventive in North America.
The discovery of a new Atheroides species in the course of general aphid collecting using a beating tray technique (i.e. not specifically targeting cryptic grass feeders such as Atheroides) suggests that directed searching for Atheroides in North America may lead to discovery of additional native species. Future field work should include accurate species identification of host plants, searching a range of habitats including extremes of altitude, latitude, and precipitation, and detailed notes on microhabitats.
The authors thank A. Carmichael, Systematic Entomology Laboratory, Beltsville, MD, for assistance in DNA extraction and sequencing; and the Valles Caldera National Preserve for logistical and field collection support. We thank K. Wieczorek for examining specimens of A. vallescaldera and commenting on their identity prior to publication. We also thank the ZooKeys editor and two anonymous reviewers for their helpful comments and suggestions. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. The USDA is an equal opportunity provider and employer.