Identity of the native South American armored scale insect species (Hemiptera: Coccomorpha: Diaspididae) widely misidentified as the North American species Diaspidiotus ancylus Putnam

Abstract

The Putnam scale, Diaspidiotus ancylus Putnam, 1878 (Hemiptera: Coccomorpha: Diaspididae), a species considered to be native to North America, has frequently been reported to be present in Chile and Argentina, attacking a wide variety of orchard crops (apples, pears, olives, nectarines, grapes) and common street trees (poplar, locust). However, diagnostic DNA sequences from Chilean populations identified as D. ancylus differ from those of North American D. ancylus; instead they are identical to those reported for Clavaspis patagonensis Schneider, Claps, Wei, Normark & Normark, 2020, a species previously known only from a single locality in Argentina. We have examined the Chilean and Argentine specimens identified as D. ancylus or Diaspidiotus sp. in major collections in Chile, France, Argentina, and United States, and we determine that nearly all of them belong to C. patagonensis and none belong to D. ancylus. Here we provide a redescription of C. patagonensis with a distribution map and a guide to distinguishing it from D. ancylus. Clavaspis patagonensis occurs throughout most of Chile, from Atacama to Aysén, and in at least 3 provinces in Argentina (Neuquen, Rio Negro, Entre Rios). Diaspidiotus ancylus apparently does not occur in Chile. We have examined specimens of C. patagonensis from 18 plant families. Field surveys of diaspidids in Chile indicate that C. patagonensis is one of the most common species of diaspidids in the country.

Introduction

Armored scale insects (Diaspididae) are the most species-rich family of scale insects (Hemiptera: Coccomorpha), with over 2,700 described species (García Morales et al. 2016). Armored scale insects spend most of their lives attached to their hostplant. For that reason—and because they are small and mostly cryptic—they are often present on agricultural and horticultural products subject to international trade, and are often introduced in new regions and become invasive (Miller et al. 2005). Many armored scale insect species have broad host ranges (García Morales et al. 2016, Kondo and Watson 2022), which may further facilitate their spread to new areas. For instance, adventive armored scale insects from abroad establish populations in the United States at a rate of about 1 species per year (Miller et al. 2005), and about 40% of the armored scale insect fauna of the United States consists of introduced species (Miller et al. 2005, García Morales et al. 2016). Many armored scale insects are economic pests, and these are disproportionately the introduced species: in the United States, about 80% of the introduced species and 20% of the native species are regarded as pests (Miller and Davidson 1990, Miller et al. 2005). In Chile, the known diaspidid fauna comprises 53 species (García Morales et al. 2016); of these, 31 are widely distributed species that are known to have originated in the Old World or in North America (Normark et al. 2019) and thus are clearly introduced in Chile. Thus, either Chile has a remarkably high proportion of introduced diaspidids (nearly 60%), or its native diaspidid fauna is relatively poorly known. One of us (PA) has been conducting surveys of the Chilean diaspidid fauna since 2015 (Amouroux et al. 2017), and has indeed found additional native species, of which one has been described so far (Amouroux et al. 2020). Here, we report another addition to the known native diaspidid fauna of Chile.

One diaspidid species that has been widely reported attacking cultivated plants in Chile is Diaspidiotus ancylus Putnam, 1878 (Aspidiotinae: Aspidotini), a species native to North America. Chilean populations identified as D. ancylus have been the focus of studies addressing their biology and potential economic impact on apples (González 1987) and on black locust (Robinia pseudoacacia) (Arancibia et al. 1990), and D. ancylus has also been reported on a wide variety of other economically important plants in Chile and Argentina, including pears, olives, nectarines, grapes, and poplar (González et al. 1973, Prado 1991, Koch and Waterhouse 2000, Zamudio and Claps 2005, González 2016). The initial survey of Chilean diaspidids (Amouroux et al. 2017) reported finding D. ancylus in 2 regions; in addition to slide-mounted specimens, that study also yielded DNA sequences for fragments of 2 gene regions, cytochrome oxidase 1 and the large ribosomal subunit (28S rDNA). Subsequently, working entirely independently from PA, another group of us (BBN, RDN, and LEC) participated in a study of diaspidids of the tribe Aspidiotini in Argentina (Schneider et al. 2020), in which we described a new species from a single site in Neuquen: Clavaspis patagonensis Schneider, Claps, Wei, Normark and Normark. That study also yielded DNA sequences, including a fragment of 28S rDNA. Shortly after that, PA noticed that the 28S sequences from Chilean ‘Diaspidiotus ancylus’ were identical to those of the type series of C. patagonensis, and BBN noticed that specimens from Chile labeled ‘Diaspidiotus sp’. in the U.S. National Museum (USNM) had the morphology of C. patagonensis. We hypothesized that C. patagonensis was widespread in Chile and that it had been chronically misidentified as D. ancylus. We set out to test that hypothesis with 28S DNA sequences from a wider sample of specimens and with a comprehensive survey of relevant museum collections. We conclude that, indeed, C. patagonensis is widespread and abundant in Chile, and we find no evidence that D. ancylus occurs in South America. Here we provide a redescription of C. patagonensis with a distribution map and a guide to distinguishing it from D. ancylus. We acknowledge that it is unusual to redescribe a species that was described so recently. It is justified in the present case because the original description was based on a very small and morphologically somewhat atypical sample, and because C. patagonensis is extremely similar to D. ancylus, such that it was necessary to study a large sample to discover the characters that are actually diagnostic of the species.

Materials and Methods

Sample Collection

Scale insect specimens were collected along a gradient from Arica in northern Chile (18° S) to Rio Puerto Tranquilo in the south (46° S), between February 2018 and December 2023. Both native and exotic plants were sampled in natural and urban areas. Specimens were preserved in 95% ethanol and stored at −20 °C.

DNA Extraction and Amplification

DNA extraction and amplification was performed as described in Amouroux et al. (2017). Briefly, the extraction was conducted without damaging the insect’s cuticle, allowing for recovery of the cuticle for morphological identification, using the prepGEM Insect DNA extraction kit (ZyGEM, Lane Hamilton, New Zealand), following the manufacturer’s recommendations. We amplified the D2 region of the large ribosomal subunit (28S). PCR was performed with a 23 μl reaction mixture based on QIAGEN Multiplex PCR buffer and 2 μl of diluted genomic DNA. The cycling conditions included initial denaturation at 95 °C for 15 min, 35 cycles of denaturation at 94 °C for 30 s, annealing at 48 °C (COI) or 58 °C (28S) for 90 s, elongation at 72 °C for 60 s, and a final extension at 72 °C for 10 min. PCR products were quality-checked via electrophoresis and then sequenced by Genewiz using an ABI 3130XL sequencer. Chromatograms were analyzed with BioEdit, and the sequences were deposited in GenBank under the accession number PQ142978 to PQ143018.

Phylogenetic Analyses

Phylogenetic analyses were conducted using 89 unique 28S haplotypes, including the 3 from this study, combined with sequences available on Genbank for all species of Clavaspis, Diaspidiotus and Hemiberlesia, other closely related genera, and a few outgroups (detailed in Supplementary data 1). Phylogenetic relationships were performed using the workflow provided by NGPhylogeny.fr (Dereeper et al. 2008, Lemoine et al. 2019). Sequences were aligned using MUSCLE (Edgar 2004) and cleaned using BMGE (Criscuolo and Gribaldo 2010). The best model was defined by SMS as GTR + G + I (Lefort et al. 2017). The phylogenetic tree was estimated using Maximum-Likelihood Phylogeny PhyML with SH-like aLRT for branch support (Guindon et al. 2010). The final tree was edited by iTOL version 7.2 (Letunic and Bork 2024).

Morphological Identification

Scale insect cuticles were mounted on microscope slides as described in Amouroux et al. (2017). In addition to mounting fresh specimens as described above, we re-examined the specimens discussed in Amouroux et al. (2017) and visited major scale insect collections in Chile (MNHN, MEUC, SAGC, SAGV), Argentina (CEIMYZA-INTA, IFML), France (LSV/Anses) and USA (USNM) and examined all the specimens from South America identified as D. ancylus or Diaspidiotus sp.

Abbreviations refer to the following collections. CEIMYZA-INTA, Colección Entomológica del Instituto de Microbiología y Zoología Agrícola, Instituto Nacional de Tecnología Agropecuaria, Hurlingham, Argentina; IFML, Colección Instituto Fundación Miguel Lillo, Tucumán, Argentina; LSV/Anses, Collection insectes et acariens, Laboratoire de la santé des végétaux—ANSES, site Montpellier, Campus Agropolis, Montferrier-sur-Lez, France; MEUC, Museo Entomológico de la Universidad de Chile (Museo Entomológico Luis Peña), Facultad de Ciencias Agronómicas, Universidad de Chile, Santiago de Chile, Chile; MNHN, Museo Nacional de Historia Natural, Santiago de Chile, Chile; SAGC, Colección Entomológico, Departamento de Laboratorios y Estaciones Cuarentenarias Agrícola y Pecuaria, Servicio Agrícola y Ganadero de Chile, Central, Lo Aguirre, Región Metropolitana de Santiago, Chile; SAGV, Colección Entomológico, Laboratorio de Entomología y Acarología, Servicio Agrícola y Ganadero Valparaíso, Valparaíso, Chile; USNM, United States National Museum, scale insect collection at the Agricultural Research Service, Beltsville, Maryland, USA.

Specimens were examined using an Olympus BH-2 or Olympus BX41TF phase-contrast microscope (Olympus America, Center Valley, Pennsylvania, USA), and measurements were made with the aid of an eyepiece reticule. An illustration was made using a Nikon Optiphot compound microscope (Nikon USA, Melville, New York, USA) with a camera lucida. Original drawings of pencil on paper were scanned and then electronically inked and edited using the SketchBook app (Autodesk, Inc., San Rafael, California, USA) on an Apple iPad Pro.

Distribution and Relative Abundance of C. patagonensis

To characterize the geographic range of C. patagonensis, we compiled the localities of all the specimens and plotted them on a map, using QGIS 3.40 (QGIS.org 2024). For samples without numerical geographic coordinates, the locality name, handwritten in the slide, was used as proxy for the graphical representation using the database GeoPortal (https://www.geoportal.cl/geoportal/catalog/36610/Topónimos). Based on the sampling described above, the materials of C. patagonensis from Chilean collections and those reported in Amouroux et al. (2017), we used the relative abundance of species in those samples to estimate their relative abundances, distributions, and host ranges in Chile. Specifically, we compared the abundance, geographic range, and host range of C. patagonensis to those of other species.

Results

A fragment of 28S rDNA was sequenced from 42 individuals from multiple hosts and localities in Chile (Table 1). Two of these were identical in sequence to a paratype of C. patagonensis and also to 2 specimens identified as ‘Diaspidiotus ancylus’ in Amouroux et al. (2017). The other 40 individuals had 1 of 2 other very similar haplotypes. The results of the phylogenetic analysis (Fig. 1) show that these 3 haplotypes form a tight clade (labeled Clavaspis patagonensis in Fig. 1) and that they are only distantly related to D. ancylus.

Table 1.

Collection data for the samples of Clavaspis patagonensis collected between 2018 and 2023. “Code” is a unique sample identifier. Latitude and Longitude are given to a precision of 20 m. “n DNA” is the number of individuals with 28S sequenced registered in GenBank and “n slide” is the number of slide-mounted specimens examined. Full information is available in GBIF, https://doi.org/10.15468/sbt4d3

Code	Latitude	Longitude	Date	Host plant			n DNA	n slide
				Family	Species	Tissue
PA812A	−33.045	−71.501	12-xii-2018	Salicaceae	Azara sp.	Leaf
PA854A	−33.823	−70.064	23-xii-2018	Euphorbiaceae	Colliguaja odorifera	Bark
PA980A	−34.302	−70.450	07-ii-2019	Rhamnaceae	Retanilla ephedra	Bark	2	2
PA983A	−34.301	−70.450	07-ii-2019	Rhamnaceae	Retanilla ephedra	Bark
PA986A	−34.304	−70.454	07-ii-2019	Escalloniaceae	Escallonia sp.	Bark
PA914A	−35.425	−71.515	28-i-2019	Rosaceae	Eribotrya japonica	Bark
S184	−35.830	−72.508	30-i-2019	Unknown	Unknown	Leaf
PA1313A	−36.789	−73.155	03-xii-2023	Anacardiaceae	Lithraea caustica	Bark
PA829A	−39.238	−71.834	19-xii-2018	Monimiaceae	Laureliopsis philippiana	Leaf
PA1003A	−41.512	−72.610	24-ii-2019	Winteraceae	Drimys winteri	Bark	2	2
PA1004A	−41.513	−72.610	24-ii-2019	Podocarpaceae	Saxegothaea conspicua	Leaf	1	3
PA1014A	−41.697	−72.113	26-ii-2019	Salicaceae	Salix sp.	Bark		3
PA891A	−46.570	−72.903	14-i-2019	Proteaceae	Embothrium coccineum	Bark	2	3
PA910A	−46.519	−73.05	14-i-2019	Nothofagaceae	Nothofagus antarctica	Bark	2
PA911A	−46.566	−72.907	14-i-2019	Nothofagaceae	Nothofagus antarctica	Bark	1
PA892A	−46.324	−73.414	15-i-2019	Winteraceae	Drimys winteri	Bark	2	4
PA894A	−46.296	−73.407	15-i-2019	Winteraceae	Drimys winteri	Leaf	2	2
PA897A	−46.297	−73.412	16-i-2019	Nothofagaceae	Nothofagus sp.	Bark	2	2
PA898A	-46.323	−73.415	17-i-2019	Nothofagaceae	Nothofagus sp.	Bark
PA899A	−46.325	−73.415	17-i-2019	Nothofagaceae	Nothofagus nitida	Bark	2
PA900A	−46.325	−73.414	17-i-2019	Ericaceae	Gaultheria sp.	Bark	2	3
PA901A	−46.327	−73.412	17-i-2019	Nothofagaceae	Nothofagus betuloides	Bark	2	3
PA902A	−46.328	−73.408	17-i-2019	Ericaceae	Gaultheria sp.	Bark	2	2
PA903A	−46.328	−73.404	17-i-2019	Winteraceae	Drimys winteri	Bark	2
PA904A	−46.351	−73.323	18-i-2019	Podocarpaceae	Podocarpus nubigenus	Bark	2	3
PA906A	−46.354	−73.328	18-i-2019	Nothofagaceae	Nothofagus betuloides	Bark	2	3
PA907A	−46.353	−73.324	18-i-2019	Nothofagaceae	Nothofagus sp.	Bark	2	3
PA908A	−46.353	−73.328	18-i-2019	Proteaceae	Embothrium coccineum	Bark	2
PA909A	−46.349	−73.321	18-i-2019	Monimiaceae	Laurelia sempervirens	Bark	2
PA910A	−46.519	−73.053	18-i-2019	Nothofagaceae	Nothofagus sp.	Bark	2	2
PA915A	−46.624	−72.677	19-i-2019	Proteaceae	Embothrium coccineum	Bark	2
TZ030	−46.624	−72.675	19-i-2019	Nothofagaceae	Nothofagus nitida	Bark	2

Fig. 1.

Consensus tree obtained by Maximum-Likelihood Phylogeny inference from 28S haplotypes of Clavaspis, Diaspidiotus, Hemiberlesia and related genera available on GenBank and from this study. Numbers on branches are posterior probabilities. Outgroup Saissetia oleae not shown.

From the morphological study of scale insects collected in Chile and Argentina that were previously identified as D. ancylus or Diaspidiotus sp. we found that nearly all specimens were more consistent with C. patagonensis than with D. ancylus. A few apparently belonged to undescribed species of Clavaspis MacGillivray, a few others to Diaspidiotus gigas (Thiem & Gerneck). None were found to represent actual D. ancylus. Collection data for specimens identified as C. patagonensis are given in Table 2. Below we present a redescription of C. patagonensis and discuss how this species can be distinguished from D. ancylus.

Table 2.

Collection data for historical slide-mounted specimens of Clavaspis patagonensis from museum collections that were examined for this study. Full names of collections are listed under Materials and Methods. Latitude and longitude were inferred from the locality name. The number of slide-mounted specimens examined is listed under “n”.

Collection	Country	Latitude	Longitude	Host plant		Date	n
				Family	Species
ANSES	Chile	−35.84	−71.62	Oleaceae	Fraxinus sp.	28-v-2015	2
IFML	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	1-i-1984	1
IFML	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	14-xii-1982	1
IFML	Chile	−33.73	−70.78	Fabaceae	Robinia pseudoacacia	28-ix-1978	1
MEUC	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	1-i-1984	1
MEUC	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	1-i-1985	1
MEUC	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	14-xii-1982	1
MEUC	Chile	−35.43	−71.67	Fabaceae	Robinia pseudoacacia	20-i-1993	12
MEUC	Chile	−33.75	−70.90	Fabaceae	Robinia pseudoacacia	21-vii-1986	1
MEUC	Chile	−34.67	−71.00	Fabaceae	Robinia pseudoacacia	22-i-1992	2
MEUC	Chile	−33.8	−70.86	Fabaceae	Robinia pseudoacacia	24-xii-1982	8
MEUC	Chile	−33.73	−70.78	Fabaceae	Robinia pseudoacacia	3-xii-1981	7
MEUC	Chile	…	…	Monimiaceae	Peumus boldus	18-ii-1967	12
MEUC	Chile	−32.61	−71.24	Monimiaceae	Peumus boldus	7-i-1967	7
MEUC	Argentina	−41.35	−71.56	Nothofagaceae	Nothofagus dombeyi	2-xii-1987	1
MEUC	Chile	−33.45	−70.67	Oleaceae	Olea europaea	1962	3
MEUC	Chile	−28.47	−71.22	Oleaceae	Olea europaea	1-vii-1990	8
MEUC	Chile	−32.20	−70.68	Oleaceae	Olea europaea	19-xi-1999	6
MEUC	Chile	−33.17	−70.89	Oleaceae	Olea europaea	20-ix-2001	2
MEUC	Chile	−41.25	−73.02	Proteaceae	Lomatia hirsuta	27-i-1965	2
MEUC	Chile	−33.72	−70.32	Quillajaceae	Quillaja saponaria	5-xi-1966	1
MEUC	Chile	−33.69	−70.11	Quillajaceae	Quillaja saponaria	28-xii-1966	5
MEUC	Chile	−33.63	−70.37	Rhamnaceae	Colletia spinosa	21-ix-1964	1
MEUC	Chile	−33.58	−70.40	Rhamnaceae	Colletia spinosa	27-ix-1967	1
MEUC	Chile	…	…	Rosaceae	Prunus persica	2-i-1995	1
MEUC	Chile	−34.67	−71.00	Rosaceae	Malus domestica	20-ii-1992	1
MEUC	Chile	−32.20	−70.68	Rosaceae	Pyrus communis	22-ii-1994	5
MEUC	Chile	−32.20	−70.68	Rosaceae	Pyrus communis	28-i-1994	12
MEUC	Chile	−32.20	−70.67	Salicaceae	Populus alba	12-ii-1994	4
MEUC	Chile	−32.75	−70.73	Salicaceae	Populus alba	14-v-1981	2
MEUC	Chile	−34.99	−71.24	Salicaceae	Populus alba	2-iii-1983	4
MEUC	Chile	−34.35	−70.96	Salicaceae	Populus alba	2-vii-1979	7
MEUC	Chile	−34.98	−71.23	Salicaceae	Salix viminalis	4-i-1983	1
MEUC	Chile	−32.20	−70.68	Salicaceae	Populus alba	4-ii-1995	4
SAG	Chile	−33.63	−70.37	Fabaceae	Robinia pseudoacacia	19-ii-1991	7
SAG	Chile	−45.57	−72.07	Hydrangeaceae	Hydrangea serrata	18-ii-2017	2
SAG	Chile	−48.12	−73.13	Nothofagaceae	Nothofagus dombeyi	16-iv-2019	14
SAG	Chile	−27.37	−70.33	Oleaceae	Olea europaea	1-iii-1998	8
SAG	Chile	−27.37	−70.33	Oleaceae	Olea europaea	1-vi-2003	3
SAG	Chile	−28.55	−70.87	Oleaceae	Olea europaea	1-viii-1998	6
SAG	Chile	−28.57	−70.82	Oleaceae	Olea europaea	1-viii-1998	7
SAG	Chile	−33.45	−70.67	Salicaceae	Populus sp.	1-xi-1999	2
SAG	Chile	−40.07	−72.88	Smilacaceae	Smilax aspera	1-ii-1994	3
SAG	Chile	−34.17	−70.74	Anacardiaceae	Schinus molle	17-vi-2008	8
SAGV	Chile	−32.75	−70.67	Oleaceae	Olea europaea	14-viii-2015	1
SAGV	Chile	−32.25	−70.93	Oleaceae	Olea europaea	20-iii-2024	8
SAGV	Chile	−32.63	−70.73	Oleaceae	Olea europaea	25-ix-2013	3
USNM	Chile	−28.57	−70.76	…	…	16-viii-1940	1
USNM	Chile	−33.45	−70.67	…	…	22-xi-1904	1
USNM	Chile	−33.73	−70.78	Fabaceae	Robinia pseudoacacia	28-ix-1978	2
USNM	Chile	−38.43	−71.23	Nothofagaceae	Nothofagus antarctica	21-xi-1968	3
USNM	Argentina	−39.60	−71.40	Proteaceae	Embothrium coccineum	12-ii-2003	1
USNM	Chile	…	…	Rosaceae	Pyrus communis	10-iv-1928	1
USNM	Chile	…	…	Rosaceae	Prunus persica	11-iii-1941	1
USNM	Chile	…	…	Rosaceae	Prunus persica	23-ii-1927	1
USNM	Chile	−34.98	−71.23	Salicaceae	Populus sp.	25-ix-1978	3
USNM	Argentina	…	…	Vitaceae	Vitis vinifera	26-iv-1935	1

Based on our samples and on museum collections, we find that C. patagonensis is widespread in Chile, ranging from Atacama Region (27° S) to Aysen Region (48° S) (Fig. 2), and is also present in at least 3 provinces in Argentina. Based on our samples, we estimate that C. patagonensis is 1 of the 4 most abundant, widespread, and polyphagous diaspidids in Chile. Specifically, we estimate the following species to be most abundant, polyphagous, and widely distributed in Chile: Aspidiotus nerii (found at 133 localities on 35 families of host plants, from 18° S to 41° S), Hemiberlesia rapax (47 localities, 16 host families, 18° S to 36° S), Hemiberlesia lataniae (46 localities, 14 families, 18° S to 34° S), and C. patagonensis (26 localities, 18 host families, 27° S to 48° S). If ordered by host range or latitudinal range rather than abundance, C. patagonensis comes second after A. nerii.

Fig. 2.

Distribution of C. patagonensis. Triangles indicate samples collected during this study and circles indicate sites represented in museum collections. Green (or dark grey) indicates a native host plant and yellow (or light grey) an introduced host plant.

Clavaspis patagonensis Schneider, Claps, Wei, Normark & Normark, 2020

See Figs. 3 and 4

Fig. 3.

Clavaspis patagonensis habitus. A) Adult female scales and settled crawlers (whitecaps) on bark of Retanilla trinervia. Photo by Patrich Cerpa. B) Two adult female scales on bark of Nothofagus antartica. Because the scales are built beneath the plant epidermis, they are highly cryptic, but their roughly circular outlines are perceptible. Photo by PA. C) Adult female with scale removed on bark of N. antartica. Photo by PA.

Fig. 4.

Illustration of slide-mounted adult female of C. patagonensis. Drawing was made using compound microscope equipped with a camera lucida (see Materials and Methods for details) This individual was collected from Olea europaea in Petrorca, Valparaíso.

Material Examined

See Tables 1 and 2.

Redescription, n=16

Morphological terminology follows Normark et al. (2019) and Miller and Davidson (2005). The abbreviations L1, L2 and L3 refer to the median, second, and third lobes, respectively. Numbers (counts) refer to one side of the body, unless stated otherwise.

Adult Female

Adult female secreting scale cover, not pupillarial. Found on bark, leaves, and fruit of hosts. Scale cover of adult female subcircular, with subcentral exuviae. On bark, scale constructed under plant epithelium, thus taking on bark color and texture (Fig. 3A and B). On leaves and fruits, scale cover gray-brown, tinged with pink, with yellowish exuviae (González 2016). Body of adult female yellow (Fig. 3C). Scale of male smaller, oval, with exuviae near anterior end (Fig. 3A). Slide-mounted adult female (Fig. 4) 1.0 to 1.5 (median 1.2) mm long, 0.8 to 1.3 (median 1.0) mm wide; broadest at mesothorax. Body outline broadly obovate. Prosoma becoming sclerotized at full maturity. Antenna simple, with one spine-like seta. Distance between antennae 220 and 310 μm. Without disc pores associated with anterior or posterior spiracles.

Lobes: Only L1 well-developed and sclerotized, slightly wider than long, inner margins parallel or slightly converging, with 0 to 1 medial notch and 1 to 2 lateral notches; median lobes usually nearly appressed, separated by an exceedingly narrow space; L2 and L3 absent.

Paraphyses: With 1 pair of paraphysis-like clavate sclerotizations between L1; with 2 clavate paraphyses immediately laterad of L1 and 2 clavate paraphyses between the setae marking abdominal segments VII and VI (ie between the positions of L2 and L3), inner paraphysis of each pair larger than outer paraphysis; paraphysis arising from lateral angle of L1 usually broadly clavate, sometimes with terminal knob directed medially.

Plates: Often inconspicuous; without plates between L1; with pair of plates on body margin near each pair of paraphyses, each plate narrowly triangular, tapering toward apex, often with slight fringe along lateral margin; body margin anterior to seta marking abdominal segment VI (ie the position of L3) usually with a series of 3 to 4 distinctive plates, each with broad base and apical microduct opening, often flanked by 1 or 2 tines. Ducts: Dorsal pygidial macroducts of 1-barred type; one macroduct present between median lobes with anterior end slightly anterior to posterior margin of anal opening; with 2 to 3 macroducts arising from first interlobular space; roughly single-file row of 4 to 7 macroducts arising from second interlobular space; 8 to 13 in marginal and submarginal areas of abdominal segment V, arising from third interlobular space; 1 to 2 submarginal macroducts present on each side of abdominal segment IV. Margin of body from mesothorax to abdominal segment III with total of 8 to 16 ducts (1 to 6 per segment) on each side, thinner and shorter than pygidial macroducts; 1 to 4 small submedial macroducts present on each side of abdominal segments I to IV. Ventral marginal or submarginal microducts present in small groups on each segment from prothorax to abdominal segment VI.

Anal opening: Positioned in posterior third of pygidium, 8 to 15 (median 11) μm in diameter, positioned about 2 anal lengths from base of L1.

Perivulvar pores: Divided into 4 or sometimes 5 groups, 2 to 7 (median 4) in each anterolateral, 1 to 6 (median 3) in each posterolateral group, and 0 to 3 (usually 0) in anterior group; 8 to 23 (median 15) pores in total.

Adult male

apterous (Fig. 5, drawings A, B, C).

Fig. 5.

Framed illustration by R. H. González of 4 life stages of C. patagonensis, labeled Diaspidiotus ancylus and mounted on the wall of MEUC. The illustration was published in González (2016). A) ventral view of male head with antenna; B) dorsal view of male head; C) ventral view of apterous male body; D) slide-mounted second-instar female; E) slide-mounted adult female; F) ventral view of first instar (crawler); G) enlargement of the adult female pygidium. Two diagnostic features of the adult female of C. patagonensis (drawings E and G) are illustrated: broad-based plates anterior to the seta marking abdominal segment VI, and more than 8 (in this case at least 9) ducts on margin of body anterior to pygidium.

DNA Sequences

Several DNA sequences of a paratype of C. patagonensis (GenBank accession numbers KY218988, MH915713, KY221285, MH916221, KY220694) and its primary endosymbiont (KY220094) have been published, as discussed in Schneider et al. (2020). DNA sequences of a specimen from Chile, originally misidentified as D. ancylus, were published by Amouroux et al. (2017): 28S (KY085529, KY085530); cytochrome oxidase I (KY085079, KY085092). DNA sequences from the present study have been submitted to GenBank under accession numbers PQ142978 to PQ143018.

Misidentifications

Clavaspis patagonensis has been consistently misidentified as D. ancylus in Chilean and Argentine collections and in publications, including the following: González and Charlin (1968), Charlin (1972), González et al. (1973), González and Barria (1983), González (1987, 2016), Charlin and Sazo (1988), Arancibia et al. (1990), Prado (1991), Sazo Rodríguez (1995), Koch and Waterhouse (2000), Claps et al. (2001), Curkovic et al. (2005), Zamudio and Claps (2005), Barrenechea Cabrera (2011), Rubio-Meléndez et al. (2011), González (2016), Amouroux et al. (2017), and—at least with respect records from Chile—Ricalde and Garcia (2013), and Wyckhuys et al. (2013).

Host Plants

We have examined specimens of C. patagonensis from 18 families of plants, including conifers (Podocarpaceae) and a wide range of angiosperms. Anacardiaceae: Schinus areira L.; Atherospermataceae: Laurelia sempervirens (Ruiz & Pav.) Tul.; Ericaceae: Gaultheria sp. Escalloniaceae: Escallonia sp.; Euphorbiaceae: Colliguaja integerrima Gill. & Hook.; Fabaceae: Robinia pseudoacacia L.; Hydrangeaceae: Hydrangea serratifolia (Hook. & Arn.) F. Phil.; Monimiaceae: Laureliopsis philippiana (Looser) R. Schodde, Peumus boldus Molina; Nothofagaceae: Nothofagus antarctica (G. Forst.), Nothofagus betuloides (Mirb.) Oerst., Nothofagus dombeyi (Mirb.) Oerst. Nothofagus nitida (Phil.) Krasser; Oleaceae: Fraxinus sp., Olea europaea L.; Podocarpaceae: Podocarpus nubigenus Lindl., Saxegothaea conspicua Lindl.; Proteaceae: Embothrium coccineum J. R. Forst. & G. Forst., Lomatia hirsuta Diels ex J. F. Macbr.; Quillajaceae: Quillaja saponaria Molina; Rhamnaceae: Colletia spinosissima J. F. Gmel., Retanilla trinervia (Gillies & Hook.) Hook. & Arn.; Rosaceae: Eriobotrya japonica (Thunb.) Lindl., Prunus persica (L.) Batsch, Pyrus communis L.; Salicaceae: Populus alba L.; Smilaceae: Smilax aspera L.; Vitaceae: Vitis sp.; Winteraceae: Drimys winteri J. R. Forst. & G. Forst.

Additional hosts of ‘Diaspidiotus ancylus’ in Chile have been reported in published accounts, with the most comprehensive list given in Claps et al. (2001). These are likely to also represent C. patagonensis, though we have not seen specimens supporting these records. If we accept these as host records for C. patagonensis, then its recorded host range comprises 27 families. Bignoniaceae: Catalpa sp.; Cannabaceae: Celtis occidentalis L.; Fabaceae: Robinia hispida L.; Fagaceae: Fagus sp., Quercus sp.; Grossulariaceae: Ribes sp.; Hydrangeaceae: Hydrangea quercifolia Bartram; Juglandaceae: Carya illinoinensis (Wangenh.) K. Koch, Juglans australis Gris.; Lauraceae: Persea americana Mill.; Magnoliaceae: Liriodendron tulipifera L.; Polygonaceae: Muehlenbeckia sagittifolia (Ortega) Meisn.; Rosaceae: Crataegus sp., Malus sylvestris (L.) Mill., Prunus armeniaca L. P. communis var. dulcis (= Prunus amygdalus Batsch); Rubiaceae: Cephalanthus occidentalis L.; Vitaceae: Vitis vinifera L.

Distribution

Chile (Atacama, Coquimbo, Valparaíso, Región Metropolitana, O’Higgins, Maule, Biobío, Araucanía, Los Ríos, Los Lagos, Aysén—Fig. 2), Argentina (Neuquén, Rio Negro, Entre Rios).

Common Names

As a species heretofore known only from its original description, C.s patagonensis has never been explicitly assigned a common name in any language. But it does have some de facto common names in Spanish: falsa escama de San Jose (González 1987), escama del álamo y acacio (Charlin and Sazo 1988), escama del acacio (Arancibia et al. 1990), and escama del álamo (González 2016). These names have apparently only ever been applied to Chilean populations identified as D. ancylus, and thus seems to have always referred to C. patagonensis. There also exist de facto common names in English, in the form of translations of the Spanish names where they appear in the titles of articles listed by online indexing services: false San Jose scale, acacia scale.

Given that we now have a more accurate understanding of the identity of the species in question, this is an opportune moment to consider what the common name ought to be. The de facto common names discussed above all have disadvantages. Each of the English names is a homonym of something else. The name “false San Jose scale’ has already been applied to at least 2 different species, Diaspidiotus ostreaeformis (Curtis, 1843) (Miller and Davidson 2005) and Diaspidiotus pyri (Lichtenstein, 1881)(Watson 2002). The name ‘acacia scale’ has been applied to Pseudotargionia glandulosa (Newstead, 1911) (Abd-Rabou 2012); also, a search for ‘acacia scale’ via the wider internet is overwhelmed by results about equipment for weighing coffee, due to the prominence of a company called Acaia whose name is frequently misspelled. In addition to the problem of homonymy, naming a highly polyphagous insect after just one or two of its many hosts can result in misunderstandings and misidentifications. Names that start with ‘false’ do not have the same practical problem, but in our view they have a subtler problem of professional narcissism: ‘taxonomy is so hard’, such names seem to say, ‘and it’s all the organism’s fault’. In place of the several existing de facto names, we suggest common names for C. patagonensis that highlight unusual features of its diet and geography without naming any specific hosts or countries: in English, austral polyphagous scale; in Spanish, escama polífaga austral.

Remarks

A confusing aspect of C.s patagonensis is that it tends to vary in 2 characters that have often been used to distinguish genera and species of armored scale insects. The first such character is the presence or absence of plates anterior to the seta marking abdominal segment VI (the position of L3). There is variation in this character even within the type series; the original description includes illustrations of one specimen (the holotype) that lacks plates entirely and another (a paratype) that has broad-based plates anterior to the seta marking abdominal segment VI (Schneider et al. 2020). The second confusingly variable character is the shape of the medial paraphysis laterad of L1. This character has traditionally been used to distinguish the genus Clavaspis (with a broad, clavate paraphysis if not an elaborate knobbed one) from Diaspidiotus and Hemiberlesia (with a simple paraphysis, only slightly wider towards the apex). The authors of C. patagonensis assigned the species to Clavaspis based on molecular-phylogenetic evidence, in spite of the type series having a relatively narrow, Diaspidiotus-like paraphysis in this position. But in this respect, the type series is somewhat atypical of C. patagonensis; most individuals across the range of the species exhibit a broader and more typically Clavaspis-like paraphysis (Fig. 4).

The original description of C. patagonensis discussed how it might be distinguished from several species of Clavaspis and Diaspidiotus, though not from D. ancylus. Instead it was compared to D. osborni, which (like the holotype of C. patagonensis) lacks plates. In practice, the species with which C. patagonensis has been consistently confused is D. ancylus. The 2 species may be distinguished as follows. In C. patagonensis, the plates anterior to the seta marking segment VI, when present, are broad-based, with a central microduct orifice often flanked by one or two tines (simple, linear plates present in this position linear in D. ancylus); the paraphysis laterad of L1 is variable, often broadly clavate, sometimes with terminal knob directed medially (always moderately developed in D. ancylus, not broadly clavate, without terminal knob); L2 is absent (L2 represented by a point, or sometimes well-developed, in D. ancylus); the body margin from thorax to abdominal segment III has 8 or more marginal ducts, narrower than dorsal ducts of pygidium, on each side (5 or fewer such ducts in D. ancylus); the anus is tiny, only 8–15, median 11 µm in length (anus small, 12 to 20, median 15 µm, in D. ancylus); and there is a total of only 8 to 23, median 15, perivulvar pores (18 to 44, median 25, in D. ancylus).

Discussion

Molecular and morphological evidence both indicate that Chilean scale insect populations previously identified as D. ancylus actually belong to the recently described species C. patagonensis. Thus, what were thought to be invasive populations of a North American species actually represent a native South American species. Clavaspis patagonensis is found on several economically important plants introduced to Chile and Argentina from the Palearctic (olives, apples, pears, nectarines, grapes, loquat, white poplar) and Nearctic (black locust) and also on a wide range of native Chilean and Argentine species (Colletia spinosissima, Drimys winteri, Embothrium coccineum, Hydrangea serratifolia, Laureliopsis philippiana, Lomatia hirsuta, Nothofagus antarctica, Nothofagus betuloides, Nothofagus dombeyi, Nothofagus nitida, Peumus boldus, Podocarpus nubigenus, Quillaja saponaria, Retanilla trinervia, Saxegothaea conspicua, Schinus areira). We estimate that C. patagonensis is 1 of the 4 most abundant diaspidid species in Chile. Diaspidiotus ancylus is absent from Chilean and Argentine collections and apparently does not occur in Chile or Argentina.

This finding has implications for plant quarantine. Clavaspis patagonensis is not a major pest of any of its hostplants, but it does occur on fruits that are subject to international trade. Blemishes caused by C. patagonensis reduce the value of apples (González 1987), and the USNM contains specimens intercepted in plant quarantine on pears and nectarines from Chile and on grapes from Argentina (Table 2). Because D. ancylus has been thought to be already established in Europe and Chile as well as the United States, it has not been considered a problem for plant quarantine in any of those regions. But as far as is now known, C. patagonensis is not established in the United States or Europe, nor is D. ancylus established in Chile or Argentina; thus, both species may merit a higher level of scrutiny and concern than they have received to date. Diaspidiotus ancylus has also been reported from Brazil (Claps et al. 2001, Culik et al. 2008, Martins et al. 2022), but we have not had an opportunity to examine any voucher specimens. It is possible that some or all of them may actually refer to C. patagonensis.

We have examined specimens of C. patagonensis from 18 plant families. An additional 9 plant families are given as hosts of ‘Diaspidiotus ancylus’ in Chile by Claps et al. (2001), an article for which the Chilean records were provided by co-author R. H. González. Since González’s concept of D. ancylus in Chile corresponds to what we now know as C. patagonensis (Fig. 5), these can be treated as credible host records for C. patagonensis. This brings the number of host plant families of C. patagonensis to 27, making its diet a case of extreme polyphagy (Normark and Johnson 2011) and placing it in the 98th percentile for diet breadth among armored scale insect species (M. García Morales, unpubl. data). Removing these host records from the recorded host range of D. ancylus does not reduce that range at all: the Chilean records of ‘Diaspidiotus ancylus’ were never indexed by ScaleNet and for the Argentine record that was indexed, D. ancylus is found on the same host in North America (García Morales et al. 2016). Only a handful of other armored sale insect species of cool-temperate latitudes have diets as broad as that reported for C. patagonensis, and most of those are considered invasive pests (Miller and Davidson 2005, García Morales et al. 2016, García Morales, unpubl. data; Normark et al. 2019): Lepidosaphes ulmi (L.), 75 families, native to Palearctic or Holarctic, invasive in South America, Australia, New Zealand; Comstockaspis perniciosa (Comstock), 46 families, native to East Asia, invasive nearly worldwide; Lopholeucaspis japonica (Cockerell), 39 families, native to East Asia, invasive in the Americas, Europe, and Australia; D. ancylus, 37 families, native to North America, invasive in Europe, Australia, and possibly South America; and Chionaspis salicis (L.), 27 families, native to Palearctic or Holarctic.

Why were Chilean populations of C. patagonensis misidentified for so long? First, we have to acknowledge that identification of armored scale insects can be difficult, and that it was substantially more difficult before the availability of DNA sequences. What we now know to be C. patagonensis was first collected in 1904, by M. J. Rivera, and was encountered several more times (mostly by US Plant Quarantine Inspectors) between 1927 and 1941 (Table 2). All of those specimens are held by USNM and all were labeled ‘Diaspidiotus sp’. The next researchers to collect C. patagonensis were R. Charlin and then R. H. Gonzalez, working together in the 1960s at MEUC. Theirs are the first specimens to be labeled D. ancylus. Many of the labels carry question marks, and (later, in 1981) on one label González notes one of the characters that distinguishes C. patagonensis from D. ancylus: ‘tiene pocos perivulvares’ [has few perivulvars]. But in publications, starting with González and Charlin (1968), these remarks are omitted. Because Charlin and González were essentially the only Chilean authorities on scale insect taxonomy for the next 50 years (González 2016), their identifications prevailed within a wider community of entomologists. The only illustration of armored scale insects displayed at MEUC depicts multiple life stages of C. patagonensis, mislabeled as D. ancylus (Fig. 5).

We had supposed that the identification error may have been influenced by the fact that C. patagonensis was found on so many introduced plants, including many of the same orchard fruits on which D. ancylus has been found in North America. But this was not the case: as of 1968, when Charlin and González first reported the presence of D. ancylus in Chile, all the specimens they had collected —or at least all those that are still held in MEUC—had come from native plants (Colletia, Quillaja, Peumus, Nothofagus; see Table 2). Possibly the identification error was influenced by the idea that D. ancylus was a particularly variable and polyphagous species. Stannard (1965) had reported that D. anyclus exhibited what is now known as polyphenism, developing distinctly different morphologies on bark vs. leaves, and he had consequently interpreted two other species (Aspidiotus howardi Cockerell and Aspidiotus comstocki Johnson) as representing leaf-forms of D. ancylus and had lumped them all together. This, too, was probably an error. Systematists have suspected that D. ancylus as currently recognized is likely to comprise multiple species (Miller and Davidson 2005), and recent molecular studies have supported that view (Schneider et al. 2018; M. García Morales and B. B. Normark, unpubl. data; see also Fig. 1 of the present article). There is good evidence that at least one species in the complex is indeed polyphenic (M. García Morales and B. B. Normark, unpubl. data), but much else about the biology and distribution of the constituent species remains unclear. In any case, it is evident that C. patagonensis is not polyphenic. We only found C. patagonensis on bark, but numerous samples in museums are labeled as having been collected from leaves and fruits, and all are morphologically similar, resembling the bark form of D. ancylus, having just a single pair of well-developed pygidial lobes.

González (1987) concluded his discussion by noting that more than 90% of agricultural pests in Chile had been introduced from the United States and Europe, whereas none of the agricultural pests found in the United States or Europe originated in Chile. (This latter assertion he put in boldface type.) Since then, molecular-phylogenetic studies have provided evidence that at least one scale insect species of global economic importance is likely to have originated in Chile—Hemiberlesia rapax (Comstock) (Amouroux et al. 2017). Clavaspis patagonensis is another polyphagous species native to Chile that is associated with economically important plants. Fortunately, it has a small enough economic impact that it is not generally considered to be a pest. It has been intercepted in plant quarantine on fruits entering the United States, but there is no evidence that it has become established anywhere outside of South America, at least not yet.

Supplementary material

Supplementary material is available at Annals of the Entomological Society of America online.

Author contributions

Benjamin Normark (Conceptualization [equal], Data curation [equal], Investigation [equal], Methodology [equal], Validation [equal], Writing—original draft [lead], Writing—review & editing [equal]), Roxanna Normark (Investigation [equal], Visualization [equal]), Mayrolin García Morales (Investigation [equal], Writing—review & editing [equal]), Lucía Claps (Investigation [equal], Validation [equal], Writing—review & editing [equal]), and Paul Amouroux (Conceptualization [equal], Data curation [equal], Funding acquisition [lead], Investigation [equal], Project administration [equal], Writing—original draft [supporting], Writing—review & editing [equal])

Conflicts of interest. None declared.