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First report of spittlebug species (Hemiptera: Cercopidae) associated with Pinus species (Pinaceae) in Mexico.

In Italy and Spain, the spittlebug Haematoloma dorsatum (Ahrens) (Hemiptera: Cercopidae) causes severe damage to natural and planted forest trees of the genera Cedrus (Pinaceae), Cupressus (Cupressaceae), Juniperus (Cupressaceae), Picea (Pinaceae), and Pinus (Pinaceae) (Roversi & Baccetti 1994; Cobos 1995). In America, there are reports of adult males of Prosapia species (Hemiptera: Cercopidae) feeding on trees, including Ilex haberi (Lundell) W. J. Hahn, I. cornuta Lindl. & Paxton, and I. opaca Soland. ex Aiton (Aquifoliaceae), and of Iphirhina quota (Distant) (Hemiptera: Cercopidae) feeding on Bourreria costaricensis (Standl.) A. H. Gentry (Boraginaceae) (Peck 1998). Whereas there are reports of North American aphrophorid spittlebugs (Hemiptera: Aphrophoridae) feeding on natural and planted forest trees as pests (Wilson 1991), there are no reports of pine-feeding Cercopidae in either North or South America.

In 2008, adult spittlebug feeding damage was observed in Mexican forests of Pinus oaxacana Mirov. nearby Nicolas Bravo (Puebla State, Mexico) and on Pinus chiapensis (Martinez) Andresen in Santa Ana Cuauhtemoc (Canada region, Oaxaca State, Mexico) (Queyla Beteta Santiago, personal communication). The impacted area and economic damage, however, were not quantified. Subsequently, a new spittlebug outbreak was reported in Mar and Jun 2015 in the municipalities of Tetela de Ocampo, Aquixtla, and Zacatlan de las Manzanas (State of Puebla, Mexico). Approximately 3,000 to 3,500 ha were afflicted. The damage was related to a symptomatology that we called "pine decline" associated with populations of adult spittlebugs resting, feeding, and mating on the foliage of Pinus trees. Nymphs were never found on those trees or on herbaceous plants in the understory.

Symptomatology of pine decline begins with drying of pine needle tips (Fig. 1A), descending down to the base of the needles. The foliage becomes yellowish, orange, or brown (Fig. 1B), and then the needles fall. These symptoms are similar to those caused by H. dorsatum (Roversi & Baccetti 1994; Cobos 1995). Symptoms occur in the middle of the rainy season when trees take on the characteristic colors; however, trees recover their foliage at the beginning of the next rainy season. This phenomenon was observed 3 times in the last years in the 3 aforementioned municipalities, but after the 3rd time, many of the trees did not recover and they died. Nevertheless, at Santa Ana, the P. chiapensis trees recovered their foliage and none died because spittlebug populations naturally declined. At Nicolas Bravo, the P. oaxacana trees recovered, probably due to an outbreak of the entomopathogenic fungus Metarhizium anisopliae (Metsch.) Sorokin (Clavicipitaceae).

In Jun through Oct 2015, we collected insects from 3 localities of Puebla State: "Acatlan" (19.85825[degrees]N, 97.83385[degrees]W) and "Rancho Alegre" (19.84278[degrees]N, 97.85611[degrees]W), both sites in Tetela de Ocampo, and "Km 68 Carretera Federal Zacatlan-Apizaco" (19.90189[degrees]N, 97.95861[degrees]W) in Zacatlan de las Manzanas. Adult spittlebugs were found on trees of Pinus pseudostrobus Lindl,, Pinus patula Schiede ex Schltdl. & Cham., and Pinus sp., and 1 adult was feeding on Rubus sp. (Rosaceae). Many insects were observed in a feeding position with forelegs extending out into the air like the Central American species Mahanarva costaricensis (Distant) (Hemiptera: Cercopidae) (Carvalho & Webb 2005) on Heliconia spp. (Heliconiaceae) (Fig. 2A, B). Mating pairs were also observed, confirming the presence of both males and females. Adults inserted the stylet into various sites on the needles selected for feeding (Fig. 2C). At abandoned feeding sites, the damage persisted, possibly due to the phytotoxic effects of salivary substances (Fig. 2D).

Several authors have described chlorosis in pasture grasses caused by the toxic effects of cercopid saliva (Taliaferro et al 1967; Valerio & Nakano 1992). On Brachiaria decumbens Stapf (Poaceae), for instance, symptoms of damage due to 1 h of exposure to cercopid feeding was first observed 3 d later, having the greatest expression 23 d later (Valerio & Nakano 1992). Cobos (1995) reported that adults of H. dorsatum stayed only a short time on Pinus pinaster Aiton after damage was observed, when adults had completed their flight period and disappeared under field conditions. This phenomenon could be similar to that found in Puebla and Oaxaca caused by the detected cercopids.

Observation and collecting efforts resulted in the detection of 3 spittlebug species in the cercopid genus Ocoaxo on Pinus host trees. The first, at Nicolas Bravo in 2008, was identified as Ocoaxo assimilis (Walker). Another group of insects collected on Pinus trees in the same year, close to the road between Oaxaca City and Pochutla City, was identified as Ocoaxo varians (Stal). Insects collected in 2015 did not match either of the aforementioned species based on external morphology and male genitalia. This additional species is now under study and is called Ocoaxo near fowleri (Lallemand).

Based on specimens deposited in the Coleccion Nacional de Insectos of the Instituto de Biologia, UNAM (CNIN) and the Coleccion de Insectos del Colegio de Postgraduados--Montecillo (CEAM), the distribution of Ocoaxo species in Mexico by state is as follows: O. varians in Guerrero, Oaxaca, Puebla, Tlaxcala, and Veracruz; O. assimilis in Oaxaca, Puebla, and Veracruz; Ocoaxo near fowleri in Ciudad de Mexico, Coahulia, Edo. Mexico, Michoacan, Nuevo Leon, Oaxaca, Puebla, Queretaro, and San Luis Potosi. All 3 species have been collected in the states of Oaxaca and Puebla, but never at the same time.

It is necessary to establish the true relationship between Ocoaxo species and pine decline, as their distributions overlap with pine forests in many states of Mexico. Nast (1950) and Fennah (1968), authors who have worked most on the genus Ocoaxo, did not discuss their biology and ecology. In fact, there are no known observations in the literature of Ocoaxo host plants. It is clear now that there are some spittlebug species associated with pine forests. However, specific host plants for nymphs are unknown, despite the extensive search for this life stage in 2015 (Jun to Dec 2015). It may be that we did not find the nymphal stage of Ocoaxo near fowleri because our efforts were focused on pines and the understory plants. We did find nymphs on grasses but these belonged to the species Prosapia ignifera Hamilton, Prosapia teapana Fennah, and Prosapia inferens (Walker) (Hemiptera: Cercopidae), and we did not see adults of Ocoaxo near fowleri emerging from any spittlemasses.

We thank Cristina Mayorga, co-curator at the Coleccion Nacional de Insectos, Instituto de Biologia, UNAM (CNIN) for the loan of Ocoaxo species materials; Thomas Atkinson for reviewing the manuscript; Luis Orlando Lopez-Zuniga at NCSU for sending literature relevant to this scientific note. This research was funded in part by the Consejo Nacional de Ciencia y Tecnologia (CONACYT), grant #308701.

Summary

The habitat and adult host plants of 3 Ocoaxo species (Hemiptera: Cercopidae) are reported for the first time. In addition, their possible link to a disorder of forest pines we called "pine decline" in Mexico is discussed. The distribution of Ocoaxo varians (Stal), Ocoaxo assimilis (Walker), and Ocoaxo near fowleri (Lallemand) is described based on museum collection specimens and field collections performed during 2015.

Key Words: Ocoaxo assimilis; Ocoaxo varians; Ocoaxo near fowleri; Pinus pseudostrobus; Pinus patula; Pinus chiapensis; phytotoxemia

Sumario

El habitat y las plantas hospederas de tres especies de Ocoaxo (Hemiptera: Cercopidae) se reportan por primera vez. Ademas, se discute una posible relacion con un trastorno de los bosques de pinos en Mexico, llamado "Declinacion de los Pinos." Se describe la distribucion de Ocoaxo varians (Stal), Ocoaxo assimilis (Walker) y Ocoaxo near fowleri (Lallemand) con base en ejemplares de museo y colectas de campo realizadas en el ano 2015.

Palabras Clave: Ocoaxo assimilis; Ocoaxo varians; Ocoaxo cerca fowleri; Pinus pseudostrobus; Pinus patula; Pinus chiapensis; fitotoxemia

References Cited

Carvalho GS, Webb MD [eds.]. 2005. Cercopid Spittlebugs of the New World (Hemiptera: Auchenorrhyncha, Cercopidae). Pensoft Publishers, Sofia and Moscow.

Cobos JM. 1995. Nota sobre la presencia de Haematoloma dorsatum (Ahrens) en pinares del Sistema Central. Boletin de Sanidad Vegetal. Plagas 21: 133-137.

Fennah RG. 1968. Revisionary notes on the New World genera of cercopid froghoppers (Homoptera: Cercopoidea). Bulletin of Entomological Research 58: 165-190.

Nast J. 1950 (1949). A revision of the genus Sphenorhina Am. & Serv. (Homoptera: Cercopidae) Bulletin Entomologique de la Pologne 19: 114-148.

Peck DC. 1998. Use of alternative food plants exclusively by adult male froghoppers (Homoptera: Cercopidae). Biotropica 30: 639-644.

Roversi PF, Baccetti C. 1994. Ecologia ed etologia di Haematoloma dorsatum (Ahrens) (Homoptera: Cercopidae). Redia 77: 133-150.

Taliaferro CM, Byers RA, Burton GW. 1967. Effects of spittlebug injury on root production and sod reserves of Coastal bermudagrass. Agronomy Journal 59: 530-532.

Valerio JR, Nakano O. 1992. Sintomatologia dos danos causados pelo adulto da cigarrinha Zulia entreriana (Berg, 1879) (Homoptera, Cercopidae) em Brachiaria decumbens Stapf. Anais da Sociedade Entomologia do Brasil 21: 95-100.

Wilson LF. 1991. Pine Spittlebug-Its Ecology and Management. United States Department of Agriculture, Forest Service. Agriculture Handbook 695.

Ulises Castro-Valderrama (1), Jesus Romero-Napoles (1), Daniel C. Peck (2), Jorge Manuel Valdez-Carrasco (1), Celina Llanderal-Cazares (1), Hiram Bravo-Mojica (1), Francisco Hernandez-Rosas (3), and Victor David Cibrian-Llanderal (1,*)

(1) Colegio de Postgraduados, Campus Montecillo. Km 36.5, Carretera Mexico-Texcoco, C.P. 56230, Texcoco, Edo. de Mexico, Mexico; E-mail: ucastro.11@gmail.com (U. C.-V.), jnapoles@colpos.mx (J. R.-N.), jvaldez@colpos.mx (J. M. V.-C.), llcelina@colpos.mx (C. L.-C.), bravomj@colpos.mx (H. B.-M.), vicillan@gmail.com (V. D. C.-L.)

(2) BioWorks, Inc., 100 Rawson Rd., Victor, NY 14564, USA; E-mail: dpeck@bioworksinc.com (D. C. P.)

(3) Colegio de Postgraduados, Campus Cordoba. Km 348, Carretera Federal Cordoba-Veracruz, C.P. 94946, Amatlan de los Reyes, Veracruz, Mexico; E-mail: fhrosas@colpos.mx (F. H.-R.)

(*) Corresponding author; E-mail: vicillan@gmail.com (V. D. C.-L.)

Caption: Fig. 1. A) Branch with initial pine decline symptoms. B) Landscape with Pinus trees affected by pine decline symptoms.

Caption: Fig. 2. A) Adult of Ocoaxo near fowleri feeding on Pinus pseudostrobus. B) Adult of Ocoaxo near fowleri feeding on Rubus sp. C) Site and damage caused by Ocoaxo near fowleri on a needle of P. pseudostrobus. D) Final damage caused by Ocoaxo near fowleri on a needle of P. pseudostrobus.
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Author:Castro-Valderrama, Ulises; Romero-Napoles, Jesus; Peck, Daniel C.; Valdez-Carrasco, Jorge Manuel; Ll
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1MEX
Date:Mar 1, 2017
Words:1668
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