ISSN 1676-6180

10 - 1 JANUARY/JUNE - 2009

Lundiana

PUBLISHED BY THE COMMITTEE FOR TAXONOMIC COLLECTIONS, INSTITUTO DE CIÊNCIAS BIOLÓGICAS, UNIVERSIDADE FEDERAL DE MINAS GERAIS. SUPPORTED BY FUNDAÇÃO DE DESENVOLVIMENTO DA PESQUISA - FUNDEP, PRO-REITORIA DE PÓS-GRADUAÇÃO/UFMG AND SOCIEDADE DE BIOLOGIA DE MINAS GERAIS.

BELO HORIZONTE BIANNUAL

Lundiana Belo Horizonte v.10 n.1 pp. 1-80 jan/jun 2009

1 Editor-in-Chief Fernando A. Silveira Universidade Federal de Minas Gerais (UFMG), BR

Editorial Board

Alexandre Salino Marcos Callisto Universidade Federal de Minas Gerais, BR Universidade Federal de Minas Gerais, BR Ângelo B. M. Machado Mario B. Figueiredo Universidade Federal de Minas Gerais, BR Instituto Biológico, BR Arturo Roig-Alsina Miguel Trefaut Rodrigues Museo Argentino de Ciencias Naturales, AR Universidade de São Paulo, BR Ary Corrêa Jr. Mônica Lopes-Ruf Universidade Federal de Minas Gerais, BR Universidad Nacional de La Plata, AR Cástor Cartelle Guerra Nico Nieser Universidade Federal de Minas Gerais, BR Tiel, NL Delir C. G. Maués-Freire Ping Ping Chen Instituto Oswaldo Cruz, BR National Natural History Museum Naturalis, NL Francisco R. Barbosa Pedro M. Linardi Universidade Federal de Minas Gerais, BR Universidade Federal de Minas Gerais, BR Geraldo W. Fernandes Rogério P. Martins Universidade Federal de Minas Gerais, BR Universidade Federal de Minas Gerais, BR Gustavo A. B. Fonseca Sérgio D. J. Pena Universidade Federal de Minas Gerais, BR Universidade Federal de Minas Gerais, BR Jacques R. Nicoli Silvana C. Thiengo Universidade Federal de Minas Gerais, BR Instituto Oswaldo Cruz, BR Jorge A. Dergam dos Santos Sílvia A. Mazzucconi Universidade Federal de Viçosa, BR Museo Argentino de Ciencias Naturales, AR José C. Motta Jr. Timothy P. Craig Universidade de São Paulo, BR University of Minnesota, USA José C. Nogueira Thomas Brooks Universidade Federal de Minas Gerais, BR Conservation International, USA Lileia Diotauti William W. Thomas Instituto Oswaldo Cruz, BR New York Botanical Garden, USA Marc A. Lachance Wiliam Ronald Heyer University of Western Ontario, CA Smithsonian institution, USA

Articles published in Lundiana are abstracted and/or indexed in: Aquatic Sciences and Fisheries Abstracts (Cambridge Scientific Abstracts), BIOSIS, CAB Abstracts, Index to American Botanical Literature (New York Botanical Garden), Kew Record (Royal Botanic Gardens, Kew), Geobase (Elsevier), SCOPUS (Elsevier), Google Scholar and Zoological Record.

Lundiana / published by the Committee for Taxonomic Collections, Instituto de Ciências Biológicas da Universidade Fede- ral de Minas Gerais. - Belo Horizonte : O Comitê, 1980 - v. : il. ; 28 cm.

Irregular: 1980-1982. Interrupted: 1982-2001. Bi-annual: From 2002 on. The first publications of Lundiana - number 1 (December 1980) and number 2 (December 1982) - had no volumes. From 2002 on, Lundiana is published in volumes (one per year). International Journal of Ornithology (ISSN 1519-888X) – last issue: vol. 4, n. 3/4 (2001); and Tangara (ISSN 1518-1723) – last issue vol. 1, n. 4 (2001) were incorporated to Lundiana in volume 4, number 1. ISSN 1676-6180

1. Biodiversity - Conservation. 2. Universidade Federal de Minas Gerais, Instituto de Ciências Biológicas. CDU: 502.74

2 Lundiana 10(1):3-10, 2009 © 2011 Instituto de Ciências Biológicas - UFMG ISSN 1676-6180 Fitossociologia em sub-bosque de Eucalyptus paniculata Smith da Lagoa do Piauzinho, Ipaba, Minas Gerais, Brasil

Leonardo C. Resende1 & Fernando A. Ferreira2 1 Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais; Av. Antonio Carlos, 6627; 31270-901 Belo Horizonte, MG, Brasil. E-mail: [email protected] 2 Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual do Paraná; Av. Colombo, 5790, PEA, Bloco G90, Jardim Universitário; 87020-590 Maringá, PR, Brasil.

Abstract Phytossociology in the understory of wood of Eucalyptus paniculata Smith at Lagoa do Piauzinho, Ipaba, Minas Gerais, Brazil. Eucalyptus is a common element in the landscapes of southeastern Brazil, with economic and forestry value, and is also the target of several controversies. In this study, floristic and phytosociologic parameters are described for the understory of an Eucalyptus paniculata wood located at La- goa do Piauzinho, municipality of Ipaba, in the Brazilian state of Minas Gerais. Sampling was done between April and May 2006, for the analysis of floristic composition, species aggregation, and horizontal, diametric and vertical structure. One hundred and one individuals belonging to 22 species of 16 families were sampled in two parcels. The most abundant species were Apuleia leiocarpa, Lecythis lurida and Casearia sp. 2. The floristic diversity of the area was low compared to those found in other similar studies. The E. paniculata wood offered adequate conditions for the development of the different successional stages, with some late- succession species starting to appear and to colonize the understory.

Keywords: floristic composition, horizontal structure, succession, sylviculture, vertical structure

Introdução florestais exóticas e comunidades florestais nativas ajuda a elucidar questões biológicas, conservacionistas e econômicas A Mata Atlântica é um dos cinco biomas mais importantes importantes (Sartori et al., 2002). do mundo, apresentando elevada diversidade de espécies da No que diz respeito à sucessão, Silva Júnior et al. (1995) flora e fauna, muitas das quais endêmicas e fortemente argumentaram que espécies de Eucalyptus podem desenvolver o ameaçadas de extinção (Mittermeier et al., 2005). Este bioma papel de pioneiras e, dessa forma, contribuir para o tem sido alterado e fragmentado pela implantação de pastagens, desenvolvimento dos estádios sucessionais avançados da floresta agricultura, silvicultura, mineração e outras atividades nativa, produzindo sombra para espécies ombrófilas, que não se econômicas (Araújo, 2000), que acabam levando à perda de desenvolvem sob incidência direta de luz. Entretanto, muitas hábitats e, consequentemente, de biodiversidade (Scariot et al., críticas são dirigidas aos eucaliptais, dificultando a conciliação 2003). Na região Sudeste, sobretudo em Minas Gerais, o entre as partes interessadas em preservar a floresta nativa e as eucalipto é um dos protagonistas destas alterações da paisagem partes interessadas em explorá-la. Segundo Lima (1996), a (Araújo, 2000). regeneração deficiente em sub-bosques de eucaliptos pode ter Neste contexto, é importante conhecer os processos duas causas: competição voraz entre as espécies por água, dinâmicos e sucessionais de uma dada área, visto que as nutrientes, luz ou outros recursos do ambiente; ou a existência alterações ou distúrbios sofridos ao longo do tempo influenciam de efeito alelopático nos eucaliptais. Ainda segundo aquele significativamente tais processos (Oliveira-Filho et al., 1997). autor, em muitos casos, a inibição do crescimento do sub-bosque Sendo assim, conhecer as interações entre plantios de essências por parte dos eucaliptais deve-se ao mau uso do solo, cujo manejo é implementado de forma errônea. Ademais, Rezende et al. (1994) explicaram que além dos efeitos alelopáticos e competição por água e nutrientes, a baixa luminosidade e a Received: 12-VIII-08 espessura da manta orgânica podem contribuir significati- Accepted: 28-VIII-11 Distributed: 13-IX-11 vamente para um baixo recrutamento de espécies oriundas do

3 Resende & Ferreira

banco de sementes e para a regeneração demorada do sub- bosque associado a plantios homogêneos, principalmente em silviculturas. O objetivo deste trabalho foi determinar a riqueza, diversidade, agregação das espécies, estrutura horizontal, diamétrica e vertical da comunidade vegetal em sub-bosque de um plantio de Eucalyptus paniculata Smith.

Material e Métodos

Área de estudo

Este estudo foi conduzido no sub-bosque de um talhão de E. paniculata Smith localizado às margens da lagoa do Piauzinho Figura 1 - Representação esquemática das parcelas amostradas no sub- bosque de um talhão de Eucalyptus paniculata, na Lagoa do (19º 26’ 25’’ W; 42º 25’ 15’’ S; 205 m de altitude), município Piauzinho, município de Ipaba, Minas Gerais, Brasil. O de Ipaba, Minas Gerais, cuja área total do plantio é de 1.089,6 ponto representa um indivíduo amostrado. ha. A região encontra-se no domínio da Floresta Estacional Semidecidual Submontana (Rizzini, 1997). O clima do local é classificado, segundo Köppen (1948), como Aw (tropical úmido de savana ou megatérmico), com um absoluta e relativa, freqüência absoluta e relativa e dominância período de chuvas e outro de estiagem bem definidos. Segundo absoluta e relativa. Além disso, foi determinado o valor de dados obtidos na estação meteorológica do viveiro florestal importância e valor de cobertura de cada espécie (Mueller- localizado em Belo Oriente (42º 23’ W; 19º 17’ S; 214 m Dombois & Ellenberg, 1974). a.n.m.), a temperatura máxima média (32,2ºC) geralmente ocorre Para a análise da composição florística foram calculados os no mês de fevereiro e a mínima média (19,4ºC), entre os meses índices de diversidade de Shannon-Weaver (H’) e equitabilidade de julho e agosto. A umidade relativa média é de 59,8%, sendo a de Pielou (J) (Pielou, 1975). Como indicador de hetero- máxima geralmente no mês de abril (aproximadamente 65%) e a geneidade, utilizou-se o coeficiente de mistura de Jentsch (QM). mínima geralmente no mês de agosto (aproximadamente 51%). Para estimativa dos parâmetros fitossociológicos e análise da A precipitação mensal média é de 106,6 mm, sendo a máxima composição florística foi utilizado o software Fitopac 2 geralmente no mês de dezembro (aproximadamente 271,1 mm) e (Shepherd, 2010). Contudo, a comparação entre as diversidades a mínima geralmente no mês de julho (aproximadamente 13,1 da Parcela 1 e Parcela 2 foi realizada através do teste t, com mm). auxílio do software PAST (Hammer et al., 2001). Para a análise de agregação de espécies foi utilizado o índice de Fracker & Amostragem Brischle (K), que considera as espécies com apenas um indivíduo, uma vez que utiliza a densidade como base para o A amostragem foi feita entre os meses de abril e junho de cálculo. O software Savan (Bortolin Júnior, 2008) foi utilizado 2006, através do método de parcelas (Mueller-Dombois & para analisar a agregação das espécies. Ellenberg, 1974). Cada parcela media 50 m ´ 10 m. Na metade da parcela foi demarcado um transecto que facilitasse a Resultados e discussão localização de todos os indivíduos amostrados (Fig. 1), para se traçar o perfil da distribuição das espécies arbóreas nativas nas Nas duas parcelas amostradas foram registrados 101 parcelas. Nas duas parcelas amostradas, todos os indivíduos de indivíduos. Entretanto, somente 73 deles puderam ser espécies arbóreas com circunferência à altura do peito (CAP) identificados, pois os demais não possuíam material fértil ou as igual ou superior a 2,5 cm (Meira-Neto & Martins, 2000) foram informações dendrométricas mínimas necessárias para mensurados e tiveram amostras coletadas. A altura de cada determinação de sua identidade. Os 73 indivíduos identificados indivíduo amostrado foi estimada tomando como referência o pertenciam a 22 espécies de 16 famílias. Dentre eles, três foram comprimento do podão. identificados somente até o nível de família e nove somente até Todos os indivíduos férteis coletados foram incorporados ao o nível de gênero (Tab. 1). Herbário do Centro Universitário do Leste de Minas Gerais As famílias com maior número de espécies foram Rutaceae (HUNL) e identificados através de comparações entre o material (3 espécies) e Anacardiaceae, Boraginaceae, Fabaceae e coletado e o material existente no HUNL, que foi classificado Salicaceae (2) (Fig. 2). As outras famílias, que correspondem a com base no sistema APG III (2009). A grafia dos nomes foi 81% do total de indivíduos registrados, foram representadas por verificada de acordo com Tropicos.org, do Missouri Botanical apenas uma espécie. Das famílias que apresentaram maior Garden (Tropicos.org, 2011). riqueza em espécies na Lagoa do Piauzinho, apenas Fabaceae esteve entre as mais diversificadas em estudos semelhantes Tratamento dos Dados realizados por Sartori et al. (2002) e Onofre et al. (2010) (em fragmentos de Eucalyptus saligna Smith, em São Paulo) e Todas as análises da estrutura vertical foram realizadas de Ferreira et al. (2007) (em sub-bosque de E. grandis W. Mill ex acordo com Mueller-Dombois & Ellenberg (1974). Os Maiden). Outras famílias cujas diversidades em espécies se parâmetros fitossociológicos estimados foram densidade destacaram nos sub-bosques estudados por esses autores foram:

4 Fitossociologia em sub-bosque de Eucalyptus paniculata

Tabela 1 - Lista das espécies registradas no sub-bosque em um talhão de E. paniculata situado na Lagoa do Piauzinho, município de Ipaba, Minas Gerais, Brasil. As espécies nomeadas com o nome da família contém espécimes que puderam ser identificadas somente em nível de família.

Anacardiaceae Lecythidaceae Astronium fraxinifolium Schott ex Spreng. Lecythis lurida (Miers) S.A. Mori Tapirira guianensis Aubl. Malvaceae Boraginaceae Luehea grandiflora Mart. Cordia sp.1 L. Meliaceae Cordia sp.2 L. Trichilia sp. P. Browne Chrysobalanaceae Moraceae Hirtella sp. L. Brosimum guianense (Aubl.) Huber Elaeocarpaceae Myrtaceae Elaeocarpaceae sp. Myrtaceae sp. Euphorbiaceae Ochnaceae Mabea fistulifera Mart. Ouratea sp. Aubl. Fabaceae Rutaceae Apuleia leiocarpa (Vogel) J.F. Macbr. Hortia arborea Engl. Platypodium elegans Vogel Hortia sp. Vand. Lamiaceae Rutaceae sp. Vitex montevidensis Cham. Salicaceae Lauraceae Casearia sp.1 Jacq. Nectandra sp. Rol. ex Rottb. Casearia sp.2 Jacq.

Euphorbiaceae, Lauraceae e Myrtaceae (representadas por da Lagoa do Piauzinho e os das outras áreas de estudo citadas apenas uma espécie na Lagoa do Piauzinho) e Asteraceae, acima podem se dever, também, ao esforço amostral Melastomataceae, Meliaceae, Rubiaceae, Solanaceae e relativamente pequeno aí realizado. Neste caso, um esforço Sapotaceae (não representadas na Lagoa do Piauzinho). amostral maior poderia revelar a presença de outras famílias de As famílias representadas pelos maiores números de plantas ausentes na amostra obtida em nosso estudo. indivíduos na Lagoa do Piauzinho foram Fabaceae (32 De qualquer forma, um aspecto interessante observado no indivíduos), Lecythidaceae (8), Salicaceae (8), Rutaceae (5) e sub-bosque de E. paniculata da Lagoa do Piauzinho foi a Boraginaceae (4) (Fig. 2). Sartori et al. (2002), obtiveram as presença de Meliaceae, Myrtaceae e Lauraceae, pois, segundo maiores riquezas nas famílias Araliaceae e Sapotaceae, respecti- vamente. Entretanto, segundo os mesmos autores, não é comum estas famílias apresentarem a maior riqueza de indivíduos em sub-bosque de eucalipto. Ferreira et al. (2007) obtiveram os maiores números de indivíduos para a família Lauraceae e Onofre et al. (2010), para as famílias Melastomataceae, Sapindaceae, Myrsinaceae, Annonaceae, Cyathaceae, Fabaceae, Rubiaceae, Euphorbiaceae, Piperaceae, Myrtaceae e Lauraceae. Há pouca coincidência entre as famílias mais diversificadas e abundantes registradas no sub-bosque do talhão de eucalipto amostrado na Lagoa do Piauzinho (este estudo) e aquelas registradas em outros estudos semelhantes (e.g. Sartori et al., 2002; Ferreira et al., 2007; Onofre et al., 2010). Isto poderia se dever a diferenças nos bancos de sementes, talvez relacionadas às composições florísticas das vegetações existentes anteriormente à implantação dos eucaliptais em cada região, já que, a colonização e os processos de sucessão ecológica de uma determinada área são diretamente afetados: 1) pela fonte e chuva de propágulos, podendo as sementes serem autóctones ou alóctones; 2) por uma contribuição significante do banco de sementes e plântulas disponíveis no solo; ou 3) ser mediada pela Figura 2 - Número de indivíduos e espécies amostradas nas duas propagação vegetativa de algumas espécies “gemíferas” (Aubert parcelas no sub-bosque de um talhão de Eucalyptus & Oliveira-Filho, 1994; Rodrigues et al., 2004). Por outro lado, paniculata, na Lagoa do Piauzinho, município de Ipaba, as diferenças encontradas entre o sub-bosque de E. paniculata Minas Gerais, Brasil.

5 Resende & Ferreira

Figura 3 - Densidade relativa (%) das espécies amostradas nas duas Figura 4 - Dominância relativa (%) das espécies amostradas nas duas parcelas no sub-bosque de um talhão de Eucalyptus parcelas no sub-bosque de um talhão de Eucalyptus paniculata, na Lagoa do Piauzinho, município de Ipaba, paniculata, na Lagoa do Piauzinho, município de Ipaba, Minas Gerais, Brasil. Minas Gerais, Brasil.

Tabarelli et al. (1994), tais famílias são típicas de estádios 0,01). Além disso, o baixo valor de H’ obtido neste estudo avançados de sucessão. O fato destas famílias não terem sido comparado a outros trabalhos realizados em condições abundantes e nem terem apresentado altos valores de riqueza, semelhantes (Carneiro, 2002; Sartori et al., 2002; Souza et al., sugerem uma transição entre estádios iniciais e tardios de 2007; Onofre et al., 2010; Alencar et al., 2011) pode se dever a sucessão (Tabarelli et al., 1994) no sub-bosque aqui estudado. diversos outros fatores, como os discutidos por Marangon As espécies que apresentaram maiores valores de densidade (1999) e Mochiutti et al. (2008): Diferenças nos estádios de relativa foram A. leiocarpa, L. lurida, Casearia sp. 2 e Cordia sucessão; discrepâncias na metodologia de amostragem; sp. 1 (Fig. 3). Contudo, Carneiro (2002) verificou que as problemas taxonômicos; dissimilaridades florísticas; idade do espécies mais abundantes foram Solanum variabile Mart., talhão; fitogeografia da região e área amostrada, entre outros. Matayba elaeagnoides Radlk., C. sylvestris Sw., Acacia velutina A média do índice de equitabilidade de Pielou (J) para as DC., Campomanesia guaviroba (DC.) Kiaersk, Esenbeckia duas parcelas foi de 0,76 (Tab. 2), semelhante aos valores febrifuga (A. St.-Hil.) A. Juss. ex Mart. e Rapanea umbellata encontrados por Carneiro (2002) (0,75) e Souza et al. (2007) (Mart.) Mez. (0,74). Por outro lado, Onofre et al. (2010) encontraram um As espécies dominantes na área amostrada foram T. valor de J igual a 0,63 para indivíduos com DAP > 5 cm e de guianensis, A. leiocarpa e H. arborea (Fig. 4), que não 0,84 para indivíduos com DAP < 5 cm e altura > 1,30 m. coincidem com as encontradas por Souza et al. (2007) e Sartori Um bom indicativo da diversidade da área amostrada é o et al. (2002). A. leiocarpa e T. guianensis estão, também, entre coeficiente de mistura de Jentsch (QM; Hosokawa, 1981). Este as que apresentaram os maiores índices de valor de importância coeficiente para o presente estudo foi de 1:2 para a Parcela 1 e e de valor de cobertura, seguidas por L. lurida (Fig. 5). As três 1:4 para Parcela 2 (Tab. 2). Isto significa que a cada 2 espécies mais abundantes desse estudo representaram 63% das indivíduos amostrados na parcela 1 uma nova espécie é espécies dominantes e, de acordo com Paula et al. (2004) e encontrada e a cada 4 indivíduos amostrados na parcela 2 uma Carneiro (2002), são, todas três, espécies de sucessão nova espécie é encontrada. secundária, o que sugere que a área amostrada estaria passando A distribuição dos 73 indivíduos analisados entre as classes por processo de sucessão e regeneração natural secundária. diamétricas (CAP) não se ajusta ao modelo J-invertido (Souza, A área basal total nas duas parcelas no sub-bosque de E. 2002), visto que a maioria dos indivíduos amostrados possuía paniculata de foi de 0,3 m2/ha e as espécies com maiores áreas circunferência entre 7 cm e 15 cm (Fig. 7). Seria esperado um basais foram T. guianensis (0,08 m2/ha), A. leiocarpa (0,06 m2/ maior número de indivíduos com CAP menor que 7 cm, uma vez ha) e H. arborea (0,05 m2/ha); as menores áreas basais foram as que as espécies presentes no talhão estariam investindo em de Cordia sp. 2, de um indivíduo da família Elaeocarpaceae e de recrutamento e não em crescimento, conforme discutido em L. grandiflora, Nectandra sp. e Ouratea sp. (0,0002 m2/ha; Fig. (Souza, 2002). Entre as espécies que apresentaram maior 6). As diferenças entre as áreas basais obtidas neste estudo e em número de indivíduos na maior classe de CAP estão A. leiocarpa outros estudos semelhantes (Sartori et al., 2002; Souza et al., (2), Hirtella sp (2). e Hortia sp (2). As espécies que 2007; Onofre et al., 2010) refletem basicamente diferenças apresentaram o maior número de indivíduos na menor classe de metodológicas, principalmente, número de parcelas e também CAP foram A. leiocarpa (5), Casearia sp. 2 (5) e L. lurida (3). indivíduos amostrados, tornando qualquer tipo de comparação A distribuição espacial dos indivíduos amostrados nas duas deste parâmetro, entre esses estudos, insignificante. parcelas pode ser visualizada na Fig. 8. Segundo o índice de A média do índice de diversidade de Shannon-Weaver (H’) Fracker & Brischle (K), A. leiocarpa, Cordia sp. 1 e L. lurida das duas parcelas foi de 1,90 (Tab. 2). Entretanto, a diversidade apresentaram distribuição aleatória, enquanto as demais delas foi significativamente diferente (t = 2,54; gl = 72,64; p = apresentaram distribuição agregada (Tab. 3).

6 Fitossociologia em sub-bosque de Eucalyptus paniculata

Figura 6 - Área basal (m2/ha) das espécies amostradas em duas parcelas no sub-bosque de um talhão de Eucalyptus paniculata, na Lagoa do Piauzinho, município de Ipaba, Figura 5 - Valor de cobertura (%) e valor de importância (%) das Minas Gerais, Brasil. espécies amostradas em duas parcelas no sub-bosque de um talhão de Euclyptus paniculata, na Lagoa do Piauzinho, município de Ipaba, Minas Gerais, Brasil.

Quanto à estrutura vertical, os indivíduos que colonizaram o talhão amostrado estão organizados da seguinte forma: 6,8% dos indivíduos estão situados no estrato inferior (altura igual ou inferior a 150 cm); 83,6% estão situados no estrato médio (entre 150 cm e 800 cm); e 9,6%, no estrato superior (altura superior a 800 cm) (Fig. 9). Distribuição semelhante foi encontrada por Souza et al. (2000) em mata de silvicultura em Viçosa, MG, onde houve um predomínio do número de indivíduos no estrato médio do fragmento florestal. Segundo Mariscal-Flores (1993), o predomínio dos indivíduos no estrato médio indica que o fragmento está em estágio de sucessão secundária. No estrato inferior predominaram as espécies A. leiocarpa (1 indivíduo), Casearia sp. 2 (1), Cordia sp. 1 (1), Cordia sp. 2 (1) e V. montevidensis (1). No estrato médio, houve predomínio de A. leiocarpa (29), L. lurida (8) e Casearia sp. 2 (6). No estrato superior a espécie com maior número de indivíduos foi Hirtella sp. (2), enquanto A. leiocarpa, Hortia arborea, M. fistulifera, P. Figura 7 - Distribuição das espécies amostradas conforme sua elegans e T. guianensis foram representadas, cada uma, por um circunferência à altura do peito (CAP), em duas parcelas no indivíduo. É interessante que Rezende et al. (1994) encontraram, sub-bosque de um talhão de Eucalyptus paniculata, na em um trabalho sobre a regeneração natural de espécies nativas Lagoa do Piauzinho, município de Ipaba, Minas Gerais, em sub-bosque de E. grandis W. Mill ex Maiden, M. fistulifera Brasil.

Tabela 2 - Diversidade florística entre as duas parcelas representadas pelo índice de diversidade de Shannon-Weaver. N = número de indivíduos amostrados; S = riqueza de espécies; ln(S) = logaritmo neperiano da riqueza de espécies; H’ = índice de diversidade de Shannon-Weaver; J = índice de equabilidade de Pielou; QM = Coeficiente de Mistura de Jentsch.

Parcela N S ln(S) H’ J QM

1 27 12 2,48 2,28 0,92 1 : 2 2 46 13 2,56 1,53 0,59 1 : 4

Total/(Média) 73 22* (2,52) (1,90) (0,76) (1 : 3)

* total da riqueza não considera a repetição de espécies entre as parcelas.

7 Resende & Ferreira

Tabela 3 - Índice de agregação de espécies calculado para área amostrada na Lagoa do Piauzinho, Ipaba, MG. Ui = parcelas em que a espécie apareceu; Ut = número de parcelas amostradas; K = Índice de Fracker e Brischle.

Espécie Ui Ut K Classificação K

Apuleia leiocarpa 2 2 0 Aleatória Astronium fraxinifolium 1 2 2,48 Agregada Brosimum guianense 1 2 3,52 Agregada Casearia sp.1 1 2 2,48 Agregada Casearia sp.2 1 2 8,73 Agregada Cordia sp.1 2 2 0 Aleatória Cordia sp.2 1 2 2,48 Agregada Elaeocarpaceae 1 2 2,48 Agregada Hirtella sp. 1 2 3,52 Agregada Hortia arborea 1 2 2,48 Agregada Hortia sp. 1 2 3,52 Agregada Lecythis lurida 2 2 0 Aleatória Luehea grandiflora 1 2 2,48 Agregada Mabea fistulifera 1 2 2,48 Agregada Myrtaceae 1 2 3,52 Agregada Nectandra sp. 1 2 2,48 Agregada Ouratea sp. 1 2 2,48 Agregada Platypodium elegans 1 2 2,48 Agregada Rutaceae 1 2 3,52 Agregada Tapirira guianensis 1 2 2,48 Agregada Trichilia sp. 1 2 2,48 Agregada Vitex montevidensis 1 2 3,52 Agregada

Figura 8 - Representação esquemática da distribuição espacial dos indivíduos amostrados em duas parcelas em um talhão de Eucalyptus paniculata, na Lagoa do Piauzinho, município de Ipaba, Minas Gerais, Brasil. Cada ponto numerado representa um indivíduo. Parcela 1: 1 e 10 Apuleia leiocarpa; 2, 3, 4, 6, 8, 14, 17 Casearia sp. 2; 5 e 13 Cordia sp. 1; 7, 20, 25 e 26 Indeterminado; 9 Nectandra sp.; 11 e 12 Hirtella sp.; 15 e 16 Brosimum guianense; 18 e 27 Vitex montevidensis; 19 Astronium flaxinifolium; 21, 29, 30 e 31 Lecythis lurida; 22 Trichilia sp.; 23 e 24 Hortia sp.; 28 Tapirira guianensis. Parcela 2: 1, 2, 4, 7, 8, 12, 13, 17, 18, 19, 20, 21, 32, 33, 39, 50, 51, 52, 53, 54, 55, 56, 57, 58, 60, 62, 64, 67 e 68 A. leiocarpa; 3 e 46 Myrtaceae; 5 e 41 Rutaceae; 6 Cordia sp. 1; 9, 10, 23, 24, 25, 26, 27, 28, 29, 31, 36, 38, 40, 42, 44, 45, 47, 48, 49, 59, 61, 66, 69 e 70 Indeterminados; 11 Casearia sp. 1; 14, 34, 63 e 65 Lecythis Figura 9 - Estratificação das espécies amostradas em duas parcelas no lurida; 15 Elaeocarpaceae; 16 Cordia sp. 2; 22 Mabea sub-bosque de um talhão de Eucalyptus paniculata, na fistulifera; 30 Platypodium elegans; 35 Ouratea sp.; 37 Lagoa do Piauzinho, município de Ipaba, Minas Gerais, Luehea grandiflora; 43 Hortia arborea. Os indivíduos com Brasil. Estrato 1: indivíduos menores que 150 cm; estrato 2: identidade indeterminada, representados por quadrados na indivíduos maiores que 150 cm e menores que 800 cm; figura, foram excluídos das análises. estrato 3: indivíduos maiores que 800 cm.

8 Fitossociologia em sub-bosque de Eucalyptus paniculata

colonizando todos os estratos amostrados juntamente com Carneiro, P. H. M. 2002. Caracterização florística, estrutural algumas outras espécies. Na Lagoa do Piauzinho, esta espécie e da dinâmica da regeneração de espécies nativas em um foi encontrada, apenas no estrato superior. povoamento comercial de Eucalyptus grandis em Carneiro (2002) sugeriu que espécies que apresentam curva Itatinga, SP. 146 pp. Dissertação (Mestrado em Ciências normal para o padrão de distribuição de altura, possivelmente, Florestais) - Universidade de São Paulo, Piracicaba. são as espécies remanescentes de antigo corte de eucalipto que, Ferreira, W. C.; Ferreira, M. J. & Martins, J. C. 2007. com a maior iluminação trazida pelo corte do eucalipto, Regeneração natural de espécies arbustivo-arbóreas no sub- começaram a investir em crescimento, deixando de investir em bosque de Eucalyptus grandis em mata ciliar, no município recrutamento. Isto pode ter ocorrido, também, no talhão de de Lavras, MG. Revista Brasileira de Biociências, 5 (1): eucalipto da Lagoa do Piauzinho, pois das 22 espécies 579-581. amostradas, 17 possuíram maior número de indivíduos entre 150 Hammer, Ø.; Harper, D. A. T. & Ryan, P. D. 2001. PAST: cm e 800 cm. São elas: A. leiocarpa, A. flaxinifolium, B. Paleontological Statistics software package for education guianense, Casearia sp. 1, Casearia sp. 2, Cordia sp. 1, um and data analysis. Palaeontologia Electronica, 4 (1): 9. indivíduo da família Elaeocarpaceae, Hortia sp., L. lurida, L. grandiflora, um indivíduo da família Myrtaceae, Nectandra sp., Hosokawa, R. T. 1981. Manejo de florestas tropicais úmidas Ouratea sp., um indivíduo da família Rutaceae, T. guianensis, em regime de rendimento sustentado. Relatório Final. Trichilia sp. e V. montevidensis. Curitiba, CNPq/IBDF/UFPr. 125 pp. A partir dos dados obtidos, conclui-se que o sub-bosque do Köppen, W. 1948. Climatologia: com um estúdio de los talhão de E. paniculata estudado está em processo de sucessão climas de la tierra. México, D.F., Fundo de Cultura secundária, em virtude das espécies encontradas como A. Econômica, 478 pp. leiocarpa, T. guianensis e H. arborea. Além disso, o Lima, W. P. 1996. Impacto ambiental do eucalipto. 2.ed. São agrupamento das espécies de E. paniculata forneceu condições Paulo, Edusp, 304 pp. adequadas para a formação de diferentes estádios sucessionais, visto que, algumas espécies de sucessão tardia estão começando Marangon, L. C. 1999. Florística e fitossociologia de área de a aparecer e colonizar o talhão. floresta estacional semidecidual visando dinâmica de espécies florestais arbóreas no município de Viçosa – Agradecimentos MG. 139 pp. Tese (Doutorado em Ecologia e Recursos Naturais) – Universidade Federal de São Carlos, São Carlos. Ao Christian Marques Rodello e ao Ricardo de Oliveira Mariscal-Flores, E. J. 1993. Potencial produtivo e alter- Gaspar, do Departamento de Ciências Florestais da Universidade nativas de manejo sustentável de um fragmento de mata Federal de Viçosa pelo auxílio na identificação das espécies e no atlântica secundária, município de Viçosa, Minas Gerais. processamento dos dados. Aos amigos Luiz Gustavo Souto 165 pp. Dissertação (Mestrado em Ciência Florestal) - Soares, Fabrício Thomaz de Oliveira Ker e Flávia Ribeiro Silva Departamento de Estudos Florestais, Universidade Federal pelo auxílio nos trabalhos de campo. de Viçosa, Viçosa. Meira-Neto, J. A. A. & Martins, F. R. 2000. Estrutura da Mata da Silvicultura, uma floresta estacional semidecidual Referências montana no município de Viçosa-MG. Revista Árvore, 24 (2): 151-160. Alencar, A. L.; Marangon, L. C.; Feliciano, A. L. P.; Ferreira, R. L. C. & Teixeira, L. J. 2011. Regeneração natural Mittermeier, R. A.; Gil, P. R.; Hoffmann M.; Pilgrim, J.; avançada de espécies arbóreas nativas no sub-bosque de Brooks, T.; Mittermeier, C. G.; Lamourex, J. & Fonseca, G. povoamentos de Eucalyptus saligna Smith., na Zona da A. B. 2005. Hotspots Revisited: Earth’s biologically Mata Sul de Pernambuco. Ciência Florestal, 21 (2): 183- richest and most endangered terrestrial ecoregions. 192. México, Conservation International, 392 pp. Angiosperm Phylogeny Group III. 2009. An update of the Mochiutti, S.; Higa, A. R. & Simon, A. A. 2008. Fitosso- Angiosperm Phylogeny Group classification for the orders ciologia dos estratos arbóreo e de regeneração natural em and families of flowering plants: APG III. Botanical um povoamento de acácia-negra (Acacia mearnsii De Wild.) Journal of the Linnean Society, 161 (2): 105–121. na região da Floresta Estacional Semidecidual do Rio Grande do Sul. Ciência Florestal, 18 (2): 207-222. Araújo, M. A. R. 2000. Conservação da biodiversidade em Minas Gerais: em busca de uma estratégia para o século Mueller-Dombois, D. & Ellenberg, H. 1974. Aims and XXI. Belo Horizonte, Unicentro Newton Paiva, 36 pp. methods of vegetation ecology. New York, Jonh Wiley & (Coleção Minas XXI). Sons, 547 pp. Aubert, E. & Oliveira-Filho, A. T. 1994. Análise multivariada Oliveira-Filho, A. T.; Mello, J. M. & Scolforo, J. R. S. 1997. da estrutura fitossociológica do sub-bosque de plantios Effects of past disturbance and edges on tree community experimentais de Eucalyptus spp. e Pinus spp. em Lavras structure and dynamics within a fragment of tropical (MG). Revista Árvore, 18 (3): 194-214. semideciduous forest in south-eastern Brazil over a five-year period (1987-1992). Plant Ecology, 131 (1): 45-66. Bortolin Júnior, S. A. M. 2008. Savan: Sistema de Análise de Vegetação Arbórea Nativa. Campanha, Alagoas: Onofre, F. F.; Engel, V. L. & Cassola, H. 2010. 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9 Resende & Ferreira

Eucalyptus saligna Smith. em uma antiga unidade de Scariot, A.; Freitas, S. R.; Neto, E. M.; Nascimento, M. T.; produção florestal no Parque das Neblinas, Bertioga, SP. Oliveira, L. C.; Sanaiotti, T.; Sevilha, A. C. & Villela, D. Scientia Forestalis, 38 (85): 39-52. M. 2003. Vegetação e flora. In: Rambaldi, D. M. & Paula, A.; Silva, A. F.; Marco-Júnior, P.; Santos, F. A. M. & Oliveira, D. A. S. (Ed.) Fragmentação de Ecossistemas: Souza, A. L. 2004. Sucessão ecológica da vegetação arbórea causas, efeitos sobre a diversidade e recomendações de em uma Floresta Estacional Semidecidual, Viçosa, MG, políticas públicas. 2.ed. Brasília, MMA/SBF, pp. 103-123. Brasil. Acta Botanica Brasilica, 18 (3): 407-423. Shepherd, G. J. 2010. Fitopac 2: manual do usuário. Pielou, E. C. 1975. Ecological diversity. New York, John Campinas: Unicamp. Wiley & Sons, 165 pp. Silva Júnior, M. C.; Scarano, F. R. & Cardel, F. S. 1995. Rezende, M. L.; Vale, A. B.; Souza, A. L.; Reis, M. G. F.; Regeneration of an Atlantic forest formation in the Silva, A. F. & Neves, J. C. L. 1994. Regeneração natural de understorey of a Eucalyptus grandis plantation in south- espécies florestais nativas em sub-bosque de Eucalyptus eastern Brazil. Journal of Tropical Ecology, 11 (1): 147- grandis e em mata secundária no município de Viçosa, Zona 152. da Mata – Minas Gerais, Brasil. In: 1. SIMPÓSIO SUL- Souza, A. L.; Cota-Gomes, A. P. & Souza, D. R. 2000. Um AMERICANO, e 2. SIMPÓSIO NACIONAL DE plano de manejo para a Mata da Silvicultura. Viçosa, RECUPERAÇÃO DE ÁREAS DEGRADADAS, Foz do Universidade Federal de Viçosa, 120 pp. Iguaçu, 1994. Anais I Simpósio Sul-Americano e II Souza, A. L. 2002. Estrutura, dinâmica e manejo de Simpósio Nacional de Recuperação de Áreas florestas: Análise estrutural de floresta ineqüiânea. Viçosa, Degradadas. Foz do Iguaçu: 1994. pp. 409-418. Universidade Federal de Viçosa, 39 p. Rizzini, C. T. 1997. Tratado de fitogeografia do Brasil: Souza, P. B.; Martins, S. V.; Costalonga, S. R. & Costa, G. O. aspectos ecológicos, sociológicos e florísticos. 2.ed. Rio de 2007. Florística e estrutura da vegetação arbustivo-arbórea Janeiro, Âmbito Cultural Ed, 747 pp. do sub-bosque de um povoamento de Eucalyptus grandis W. Rodrigues, R. R.; Martins, S. V. & Barros, L. C. 2004. Tropical Hill ex Maiden em Viçosa, MG, Brasil. Revista Árvore, 31 rain forest regeneration in na area degraded by mining in (3): 533-543. Mato Grosso State, Brazil. Forest Ecology and Tabarelli, M.; Villani, J. P. & Mantovani, W. 1994. Estudo Management, 190 (2-3): 323-333. comparativo da vegetação de dois trechos da floresta Sartori, M. S.; Poggiani, F. & Engel, V. L. 2002. Regeneração secundária no Núcleo Santa Virgínia, Parque Estadual Serra da vegetação arbórea nativa no sub-bosque de um do Mar, SP. Revista do Instituto Florestal, 6 : 1-11. povoamento de Eucalyptus saligna Smith. localizado no Tropicos.org. 2011. Missouri Botanical Garden. www. Estado de São Paulo. Scientia Forestalis, (62): 86-103. tropicos.org. Acessado em 08/08/2011.

10 Lundiana 10(1):11-18, 2009 © 2011 Instituto de Ciências Biológicas - UFMG ISSN 1676-6180 Phoresy and commensalism of Chironomidae larvae (Insecta: Diptera) in the state of Rio de Janeiro, Brazil

Ana Lucia Henriques-Oliveira1,2 & Jorge Luiz Nessimian1 1 Lab. de Entomologia, Departamento de Zoologia, Instituto de Biologia, CCS, Universidade Federal do Rio de Janeiro, Ilha do Fundão, CP 68044, CEP 21944-970 Rio de Janeiro, RJ. 2 – [email protected]

Abstract: Chironomid larvae are frequently found living in phoretic or commensal association with aquatic animals in all regions of the world. In Brazil, new records have been available in the literature in the last years mainly for the state of São Paulo. In collects performed in several streams and rivers in the state of Rio de Janeiro and bordering areas, chironomid larvae were found living in association with Corydalidae (Megaloptera); Perlidae (Plecoptera); Leptophlebiidae (Ephemeroptera); Aeshnidae and Libellulidae (Odonata); Sericostomatidae (Trichoptera); Elmidae (Coleoptera) and catfishes of the families Trichomicteridae and Loricariidae (Pisces). These new records are presented in the present study.

Keywords: Chironomidae, Nanocladius (Plecopteracoluthus), Phoresy, Rheotanytarsus, symbiotic associations.

Introduction In Brazil, although still limited, new records have been published in the last years: Ichthyocladius sp. (Orthocladiinae) Associations between two organisms may range from simple on fishes of the families Astroblepidae and Loricariidae phoresy to commensalism and parasitism (Giberson et al., 1996). (Freehofer & Neil, 1967; Fittkau, 1974; Mendes et al., 2004, Phoresy is the interrelationship between two organisms in which 2007; Sydow et al., 2008); Nanocladius (Plecopteracoluthus) one is carried on the body of the other, does not necessarily sp. on Plecoptera (Dorvillé et al., 2000) and Ephemeroptera implying interdependency between both (Epler & De La RosA, (Callisto & Goulart, 2000; Pepinelli et al., 2009); 1995). In parasitism, one observes an apparent benefit to the Thienemanniella on Megaloptera (Callisto et al., 2006); parasite in form of resources being diverted from the host body, Rheotanytarsus on Odonata (Ferreira-Peruquette & Trivinho- while in commensalism the nature of the benefit to a commensal Strixino, 2003; Rosa et al., 2009), and Coleoptera (Segura et al., species is less clear. However, there is a logical difficulty in 2007). Roque et al. (2004) listed new occurrences of phoretic assuming that commensals receive no significant benefit from Chironomidae-larvae living on different aquatic animals, mainly association with the host (Tokeshi, 1993). for the state of São Paulo. In the state of Rio de Janeiro, only the Differently from other groups of aquatics insects, phoretic association of Nanocladius (Plecopteracoluthus) sp. and representatives of Chironomidae and Simuliidae (Diptera) might Kempnyia tijucana Dorvillé & Froehlich, 1997 (Perlidae) was be widely distributed. Phoretic simuliid larvae are known from recorded (Dorvillé et al., 2000). Central Asia and Tropical Africa (Moor, 1999). Chironomid In collects carried out in the state of Rio de Janeiro and larvae frequently live in association with aquatic animals in adjacent areas, chironomid larvae were found living on aquatic several parts of the world. Chironomid associations were insects (Ephemeroptera, Odonata, Plecoptera, Megalotera, recorded mainly in Europe, Asia, and Central and North Coleoptera and Trichoptera) and fishes of the families America, with larvae living on Ephemeroptera (e.g. Svensson, Trichomicteridae and Loricariidae. Here, these phoretic and/or 1980; Jacobsen, 1998), Plecoptera (e.g. Steffan, 1965; Dosdall commensal relationships are described as a contribution to the & Mason, 1981; Giberson et al., 1996), Odonata (e.g. White & knowledge of the associations between Chironomidae and their Fox, 1979; White et al., 1980, Dosdall & Parker, 1998), hosts. Hemiptera (e.g. Roback, 1977), Megaloptera (e.g. Tracy & Hazelwood, 1983; De La Rosa, 1992; Epler & De La Rosa, Material and methods 1995; Hayashi, 1998; Pennuto et al, 2002), Trichoptera (e.g. Gallepp, 1974; Kobayashi et al., 2003) and Gastropoda (e.g. The studied material derived from collects carried out in Mancini, 1979). several rivers and streams in the state of Rio de Janeiro (RJ) and adjacent areas in the states of Minas Gerais (MG) and São Paulo (SP), between 1996 and 2006 (Table I). For identification, the Received: 25-VI-08 Chironomidae larvae were removed from their hosts and Accepted: 10-I-09 mounted on permanent slides using Euparal© as the mounting Distributed: 13-IX-11 medium. The larvae were identified under an optical microscope

11 Henriques-Oliveira & Nessimian

(1000 X), using the keys by Cranston et al. (1983) and Epler Nanocladius recorded here was attached to the dorsolateral area of (1995), and taxonomic descriptions by Steffan (1965), Epler the abdomen, above the gills of its host, with its head near the host (1986), Hayashi (1998) and Mendes et al. (2004). The wingpads, and was involved in a silk layer with small particles of specimens identified are deposited in the Coleção Entomológica organic matter adhered. Jacobsen (1998) found evidences of Prof. José Alfredo Pinheiro Dutra, Departamento de Zoologia, parasitism in the association of Nanocladius with Thraulodes. He Instituto de Biologia at the Universidade Federal do Rio de observed the presence of haemolymph in the gut contents of the Janeiro (RJ). larvae and scars on the host tegument where the larva was attached. However, this was not observed in the present study. Results and Discussion Plecoptera: Phoretic associations involving species of Anacroneuria Klapálek, 1909 and Kempnyia Klapálek, 1914 The associations involving chironomid larvae presented in (Perlidae) were recorded. Nymphs of Anacroneuria (n = 3) and this study (listed in Table I) are discussed below: Kempnyia (n = 18) were found in phoretic association with Odonata: Chironomid larvae were found in association with larvae of Nanocladius (Plecopteracoluthus) (Orthocladiinae). Rhionaeschna punctata (Martín, 1908) (Aeshnidae), Elasmo- The associations were observed in nymphs of Kempnyia themis cannacriodes (Calvert, 1906) and Brechmorhoga Kirby, colossica Navás, 1934, ranging between 19 mm and 35 mm in 1894 (Libellulidae). Two nymphs of R. punctata (Aeshnidae) length, and Kempnyia sp., between 10 mm and 16 mm in length. collected in an Aiuruoca River first order tributary in the Itatiaia The nymphs of Kempnyia were collected in the Aiuruoca River National Park (in the states of Rio de Janeiro and Minas Gerais) (3rd order, 1860 m a.s.l), in a second-order tributary of this same contained, each one, a tube with a larva of Rheotanytarsus river at the Itatiaia massif, in the Mantiqueira moutain range Thienemann et Bause, 1913 (Chironominae: Tanytarsini). The (2200 m a.s.l.), between the municipalities of Itamonte (MG) stream was approximately 50 cm wide, running adjacent to a and Itatiaia (RJ), and in the Cascatinha River, Nova Friburgo forested area at 1500 m a.s.l. There, the dominant aquatic plants (RJ) (3rd order ,1300 m a.s.l.). In all of these rivers the nymphs are Senecio icoglossus DC. (Compositae) and Cyperaceae. The were collected in riffle areas (litter and stones). Anacroneuria larval tubes of Rheotanytarsus were attached to the ventral nymphs 10 mm to 13 mm in length, each with a single region, longitudinally to the external area from the prosternal Nanocladius (Plecopteracoluthus) larva, were collected in riffle region to the first abdominal segment (Fig. 1-A). The larvae had litter in the Mambucaba River and in the Boqueirão stream, both their heads and thoraxes oriented laterad in the tube, allowing in the Serra da Bocaina National Park (RJ and SP). food capture, as Rheotanytarsus larvae are primarily filterers of About 75% of the Nanocladius (Plecopteracoluthus) sp. organic matter in suspension in the water column. Similar larvae observed were close to the thoracic gills of the host observations were reported by Rosa et al. (2009) in nymphs of nymphs, and approximately 38% of the Kempnyia nymphs had Calopterygidae and Heteragrion in Minas Gerais state. two or three individuals attached to them (Fig. 1-C). Two Tubes of Rheotanytarsus larvae, some of which empty, were morphospecies of N. (Plecopteracoluthus) were observed living observed on nymphs of E. cannacriodes and Brechmorhoga sp. in association with stoneflies. Nanocladius (Plecopteracoluthus) (Libellulidae) collected in the Ubatiba river, Maricá (RJ) sp.1 were found living all their larval life among the tracheal (potamal section) at 30 m a.s.l. This river section was about 2 m gills of the host, producing at the end of the fourth instar a fine wide and its riparian vegetation was strongly modified, being silk bag among the gills for pupation. Two pupae and two pre- characterized by pastures and some shrubs. The nymphs were pupae were observed in these bags. One pair of small sclerotized collected in riffles (gravel and stones) and in pools. Rheo- hooks occurs in the abdominal sternites I-V of the larvae of this tanytarsus tubes were attached to their hosts on the legs, near the morphospecies. These larvae appear to hold themselves to the head, and between the wingpads, suggesting the lack of a host tracheal gills by their posterior parapods; no bag or tube for preferential attachment place. White et al. (1980) observed that fixation was observed in the larval stage. This morphospecies the head, thorax and legs were the main regions of Macromiidae was observed on both Anacroneuria and Kempnyia nymphs. nymphs used for fixation by chironomid larvae. Ferreira- The larvae of N. (Plecopteracoluthus) sp.2 were found only Piruquette & Trivinho-Strixino (2003) also found E. in Itatiaia, in two species of Kempnyia. These are big larvae and cannacrioides nymphs with Rheotanytarsus tubes attached to the were found under the host wingpads, during the first instars. same regions of the host body. These authors related this fact to Differently from N. (Plecopteracoluthus) sp.1, this mor- the life style of E. cannacrioides, whose nymphs cling on the phospecies do not possess small hooks on its abdominal substrate, and which abdominal expansion-contraction segments. Larvae of the fourth instar were observed only on the movements make fixation difficult for chironomid larva. Among ventrolateral surface of the host thorax, suggesting that during the hosts observed here, only nymphs of R. punctata presented this instar, the larva migrates to the ventral region for pupation. chironomid tubes attached to the ventral region of their bodies. It first adopts an inverted-J shape, thus positioning itself along Ephemeroptera: One association with Thraulodes Ulmer, the longitudinal axis of the host body (Fig. 1-D). Dorvillé et al. 1920 (Leptophlebiidae) was found. Nymphs of Thraulodes are (2000) recorded the same habit in a species of N. (Plecoptera- abundant in rocky-bedded streams in the Bocaina mountain range. coluthus) on K. tijucana. Two individuals of K. colossica were However, among several observed nymphs, only one, collected in also collected bearing larvae of both morphospecies of riffle litter in the Mambucaba River, in the Serra da Bocaina Nanocladius (Fig. 1-C). National Park, showed association with Nanocladius Megaloptera: Associations with Corydalus Latreille, 1902 (Plecopteracoluthus) sp. Steffan, 1965 (Orthocladiinae) (Fig. 1-B). (Corydalidae) were observed. Phoretic or commensal The association between species of these genera was only recently associations between Chironomidae and Megaloptera (dobsonfly recorded in Brazil (Callisto & Goulart, 2000). The larva of and fishfly) are known from Central and North America (Epler

12 Phoresy and commensalism of Chironomidae larvae

Table 1 - New occurrences of Chironomidae larvae in phoresy in the state of Rio de Janeiro and localities in bordering states. I- Chironomidae larva of first and second instars; M –Chironomidae mature larva; P – pupa. P.N. = National Park.

Host Ind. collected Chironomidae Instar Ind./host Host position Locality Tube on the ventral region Aiuruoca River R. punctata 2 Rheotanytarsus I, M 1 between the forelegs and tributary, fi rst abdominal segment. Itamonte, MG Empty tube in abdominal E. cannacrioides 3 Rheotanytarsus -1 dorsal region. Ubatiba River, Maricá, RJ Brechmorrhoga 1Rheotanytarsus I 1 Tube between wingpads. Mambucaba River, On the abdominal dorsal Thraulodes sp. 1 Nanocladius (P.) sp.3 M 1 S.José do Barreiro, region up the tracheal gills. SP Boqueirão Stream, Individuals in thoracic gills Anacroneuria 1 Nanocladius (P.) sp.2 I 1 S.José do Barreiro, fi laments SP Mambucaba River, Anacroneuria 2 Nanocladius (P.) sp.2 I 1 In thoracic gills fi laments S.José do Barreiro, SP K. colossica 5 Nanocladius (P.) sp.1 I 1 - 2 In thoracic gills fi laments Aiuruoca River, Under wingpad and gills of Kempnyia sp. 2 Nanocladius (P.) sp.2 M 1 –Itamonte, MG middle legs

Nanocladius (P.) sp.1 I, M, P 1 - 3 Thoracic gills Aiuruoca River K. colossica 5 Ventral region of the thorax, tributary, Itamonte, Nanocladius (P.) sp.2 I, M 1 one larva in ‘U’ position MG Individuals in thoracic gills Kempnyia sp. 6 Nanocladius (P.) sp.1 I, M 1 - 8 fi laments Cascatinha River, In tracheal gills fi laments in Nova Friburgo, RJ Corydalus 3 Corynoneura I, M 2 - 4 abdomen In tracheal gills fi laments in Preto River tributary, Corydalus 2 Corynoneura I1 abdomen Itatiaia, RJ Tube attached on caddisfl ies Sertão River, Parati, G. grumicha 4 Rheotanytarsus I1 case RJ Stream in Barreirinha Tube attached in ventral farm, M. granosa 3 Rheotanytarsus M, P 1 region from prothorax to P.N. Serra da abdominal segments. Bocaina, S.José do Barreiro, SP Ventral region between Barra Branca Stream, Cylloepus 3 Rheotanytarsus M, P 1 prothorax and abdominal S.José do Barreiro, segments, and one on elytra SP Barra Branca Stream, Heterelmis 2 Rheotanytarsus - 1 Tube attached on elytra. S.José do Barreiro,, SP. Preto River, P. rudolphi 32 Ichthyocladius lilianae I, M 1 - 4 Skin and on fi ns Maromba, Itatiaia, RJ Fins and odontoid plate in River in Visconde de T. mirissumba - Ichthyocladius lilianae I, M 1-3 opercula Mauá, Resende, RJ

13 Henriques-Oliveira & Nessimian

Figure 1 - A) Rhionaeschna punctata nymph with Rheotanytarsus larva attached on ventral region; B) Thraulodes sp. nymph with Nanocladius (Plecopteracoluthus) sp. larva on laterodorsal region; C) Kempnyia colossica nymph with two larvae of different morphospecies of Nanocladius (P.) on ventral region; D) Kempnyia sp. nymph with Nanocladius (P.) sp.2 larva on ventral region; E) Corydalus sp. larva with Corynoneura larvae attached to tracheal gills filaments; F) Corydalus sp. larva with last instar Corynoneura larva inside silk cocoon.

14 Phoresy and commensalism of Chironomidae larvae

& De La Rosa, 1995; Pennuto et al., 2002; Pennuto, 2003), Asia presenting commensal or phoretic relationships with (Hayashi, 1998) and from the Brazilian states of São Paulo, Chironomidae. Minas Gerais and Amazonas (Roque et al., 2004; Callisto et al., Trichoptera: Chironomid larvae were found in association 2006). Corydalus larvae carrying Chironomidae were collected with Grumicha grumicha (Vallot, 1855) (Sericostomatidae). in riffles in a 2nd order tributary of the Cascatinha River, in Nova Five specimens of G. grumicha were found carrying, each, one Friburgo (RJ), at 1300 m a.s.l. (three individuals) and in a larval tube of Rheotanytarsus. The larvae of G. grumicha were tributary of the Preto River, Itatiaia (RJ), at 1600 m a.s.l. (two collected in the Rio do Sertão, a stream in the Bocaina Mountain individuals). The Corydalus larvae were approximately 19 mm Range, Parati (RJ), at 943 m a.s.l. (Fig. 2–D). Three tubes had long, and carried two to four small Corynoneura larvae of Rheotanytarsus and two were empty. Rheotanytarsus (Orthocladiinae) larvae under their tracheal-gill filaments (Figs. tubes were attached with their openings directed towards the 1-E and 1-F). These larvae probably were in the first or second anterior opening of the host case. Grumicha individuals are developmental instars. Corynoneura larvae were observed with scrapers and normally are found on stones or litter in riffles, part of their abdomens under the abdominal gills of the host, moving on the substrate in search of food. This habit may favor with the thorax and head free. The associations recorded here are the Rheotanytarsus larval mode of life, facilitating their in accordance with the observations made by Tracy & positioning in the river current and promoting a more efficient Hazelwood (1983) that most of the chironomid larvae on filtration. The Chironomidae larvae could feed on the suspended corydalid larvae are found on the abdominal region, close to the biofilm resulting from the scraping of stone surface by Grumicha host gills. Epler & De La Rosa (1995), studying associations larvae. Ashe et al. (2000) presented a summary of chironomid- between Corydalus and Tempisquitoneura (Corynoneurini- trichopteran associations (phoretic, commensal or ectoparasitic), but group) larvae, verified that small phoretic larvae were usually there were no records for the Neotropical region. found attached among the abdominal gills of the host, while Pisces: Associations of Chironomidae with Trichomycterus larger larvae preferred the thorax and first abdominal segments. (Trichomycteridae) and Pareiorhina (Loricariidae) were The Corydalus gills seem to be a safe site for Corynoneura observed. Individuals of T. mirissumba Costa, 1992 development, hidden from predators (Callisto et al., 2006). (Trichomycteridae) and P. rudolphi (Ribeiro, 1911) These latter authors found Corydalus larvae carrying one up to (Loricariidae) were observed carrying larvae of Ichthyocladius 33 Corynoneura larvae attached mainly to abdominal segments, lilianae Mendes, Andersen & Saether, 2004 (Orthocladiinae) under gills. According to Tracy & Hazelwood (1983), other (Fig. 2-E e F), in the Preto river located at 1600 m a.s.l, in factor favoring this positioning could be the rhythmic movement Visconde de Mauá (municipality of Resende, RJ). Larvae of I. of the gill tufts, which could provide a constant source of lilianae were found on T. mirissumba inside a small gelatinous oxygen-rich water to the chironomid larvae. case composed by silk and small particles of organic matter Coleoptera: Associations were found of Tanytarsini larvae attached on the odontoid plate of the fish opercula. Frequently, with Cylloepus Erichson, 1847, Heterelmis Sharp, 1882 and more than one larva were found living in the same specimen of Macrelmis granosa (Grouvelle, 1896) (Elmidae). Eight adult T. mirissumba. In P. rudolphi (Loricariidae), one to five larvae individuals of Elmidae were collected in streams at the Bocaina of I. lilianae were found living on several parts of the body of Mountain Range, between 1000 m a.s.l. and 1200 m a.s.l., the same individual, mainly on fins. According to Fittkau carrying tubes of Rheotanytarsus: Three individuals of (1974), chironomid larvae attach to fish skin by their anal Macrelmis granosa, three Cylloepus sp. and two Heterelmis sp. parapods and, by the end of the fourth instar, they build up a The specimens of M. granosa had Rheotanytarsus tubes attached pupal case, usually attached to the fin or to the interopercular on their ventrolateral region, between the prosternum and the bristle, where they complete their development. Sydow et al. abdominal segments I-IV (Fig. 2-A). One individual of (2008), studying associations between loricariid fishes and I. Cylloepus had two tubes attached: One of them was empty on lilianae found a major preference by the later for the fin. the elytra, and the other, with one larva, was attached to the According to them, this fact would be associated to the fin ventrolateral region of the thorax with the opening near the movements, which create a favorable microhabitat for the elmid head (Fig. 2-B). A small percentage of adult individuals of Ichthyocladius larvae, that are filterer-collectors, feeding Heterelmis were found carrying Tanytarsus larvae. Among 74 mainly of algae. Another factor pointed out by the same specimens collected in a stream, only two possessed authors, is that loricariid fishes move quickly in lotic Rheotanytarsus tubes. Each one of those specimens had an ecosystems, fixing themselves to small and medium-sized empty, “U”-shaped tube attached to the pronotum and elytra. rocks where they feed on the peryphitic biofilm by grazing Roque et al. (2004) pointed out that the smooth tegument of rock surfaces. The suspending biofilm may be helpful for I. host Coleoptera would make it difficult for phoretic chironomids lilianae feeding. In the Neotropical region, species of to attach. This fact may be contributing to the absence of Ichthyocladius were recorded in Venezuela, Guyana, Bolivia, phoretic associations with specimens of other families of Peru, and in the Brazilian states of Amazonas, Mato Grosso, Coleoptera. The rugosity and punctures of the elmid pronotum, Minas Gerais, São Paulo and Rio Grande do Sul (Fittkau, elytra and venter, associated to the occurrence of these beetles in 1974; Roque et al., 2004, Sydow et al., 2008). stream riffles, may contribute to the attachment of Rheotany- tarsus tubes. Moreover, the mobility of the elmid adults Obligate or casual relationships: Tokeshi (1993) argued facilitates filtering by Rheotanytarsus larvae. Elmid adults live that, in the absence of detailed ecological information, the preferentially on rock or litter substrates in riffles, the same distinction between obligate and accidental associations is often habitat inhabited by Rheotanytarsus larvae. At the moment, the difficult to make and some relations may be trivial. The exact Elmidae is the only known representative of Coleoptera relationship between chironomid larvae and their hosts is

15 Henriques-Oliveira & Nessimian

Figure 2 - A) Adult of Macrelmis granosa with Rheotanytarsus tube on ventral region; B) Adult of Heterelmis sp. with Rheotanytarsus tube on elytra; C) Adult of Cylloepus sp. with two Rheotanytarsus tubes, one on dorsal region and other on ventral region. D) Grumicha grumicha case with Rheotanytarsus tube; E & F) Individuals of Pareiorhina rudolphi with Ichthyocladius lilianae larvae on the fin and skin.

16 Phoresy and commensalism of Chironomidae larvae

uncertain and still little known, needing specific studies. Acknowledgments Obligate relationships, such as that between Nanocladius (Plecopteracoluthus) and their hosts, need a tight synchro- The authors are grateful to ICMBio, Parque Nacional da nization between host and commensal, since the pupation or Serra da Bocaina and Parque Nacional de Itatiaia for collect adult emergence of the host may cause the death of its guests permits; to Conselho Nacional de Desenvolvimento Científico e (Pennuto, 2003). In the literature, N. (Plecopteracoluthus) larvae Tecnológico (CNPq, Brazil) for the financial support, and to the are considered relatively ‘generalist’ commensals, which Laboratório de Ictiologia Geral e Aplicada of the Departamento maintain associations with Plecoptera, Ephemeroptera and de Zoologia, Instituto de Biologia of the Universidade Federal Megaloptera. According to Fittkau (1974), species of do Rio de Janeiro, for donation of specimens of Ichthyocladius Ichthyocladius live obligatorily associated with vertebrate hosts. for identification and study; to Dr. Maria Inês da Silva dos Until now, there are no records in the literature of Passos for Elmidae identification; to Dr. Angela Mansolillo Ichthyocladius larvae living free on other substrate. Sanseverino and the anonymous referee for corrections and Obligatory associations were not observed for Rheotanytarsus suggestions that improved the manuscript. larvae, which can be observed living on riverbed substrates or as phoretic or commensals associated with several groups of aquatic References insects. Their hosts, elmid beetles (adults and larvae) and sericostomatid caddisflies (larvae), live in riffle areas (rock or litter), Ashe, P.; O’Connor, J.P. & Murray, D.A. 2000. Larvae of have scraper habit, feed on periphyton (Merritt & Cummins, 1996) Eurycnemus crassipes (Panzer) (Diptera: Chironomidae) and their movements to scrape would suspend particles that could ectoparasitic on prepupae/pupae of Hydropsyche siltalai be used as food by Rheotanytarsus larvae. These larvae are Döhler (Trichoptera: Hydropsychidae), with a summary of frequently found living in substrates as rocks in riffle areas, in known chironomid/trichopteran associations. Spixiana, 23: 267-274. accordance with the comments of Tokeshi (1993) and Hayashi (1998). According to Tokeshi (1993), the main factor governing the Callisto, M. & Goulart, M.D.C. 2000. Phoretic association host choice by species of Rheotanytarsus would be the availability between Nanocladius (Plecopteracoluthus) sp. (Chirono- midae: Diptera) and Thraulodes sp. (Leptophlebiidae: of a large body, with an exposed surface to attach their filter-feeding Ephemeroptera). Anais da Sociedade Entomológica do tubes and also able to promote protection against predators. In some Brasil, 29: 605-608. cases, as verified for nymphs of Brechmorhoga, the association can Callisto, M.; Goulart, M.; Moreno, P. & Martins, R.P. 2006. be accidental, therefore the chironomid larvae were found on Does predator benefits prey? Comensalism between Coryno- individuals with adhered organic matter and little mobility. neura Winnertz (Diptera: Chironomidae) and Corydalus Hawking & Watson (1990) pointed out that some chironomid Latreille (Megaloptera:Corydalidae) in Southearstern Brazil. larvae (Rheotanytarsus) need a steady platform for support and Revista Brasileira de Zoologia, 23: 569-572. access to a constant and abundant source of food, besides organic Cranston, P.S.; Oliver, D.R. & Sæther, O.A. 1983. The larvae matter for tube construction. of Orthocladiinae (Diptera: Chironomidae) of the Holartic The exact factors guiding host choice are unknown for the region - keys and diagnoses. In: T. Wiederholm (ed.). associations between Corydalus and the Corynoneura-group Chironomidae of the Holartic region. - Keys and diagnose. larvae. Hayashi (1988) pointed out that the large bodies of the Part I: Larvae. Entomologica Scandinavica Supplement, Megaloptera used as hosts by chironomid larvae would decrease 19: 149-291. their risk of being preyed. Although it is not known how De La Rosa, C.L. 1992. Phoretic associations of Chironomidae chironomid larvae find their hosts and colonize them, the (Diptera) on Corydalidae (Megaloptera) in northwestern searching process may limit the complexity of commensal life Costa Rican streams. Journal of the North American cycle, being dependent no host density (Hayashi, 1998). Some Benthological Society, 11: 316-323. authors (Tokeshi, 1993; Roque et al., 2004) pointed out that Dorvillé, L.F.M.; Nessimian, J.L. & Sanseverino, A.M. 2000. these interactions may benefit the Chironomidae by decreasing First record of symphoresy between nymphs of the stonefly predation risks, increasing mobility, improving protection from Kempnyia tijucana (Plecoptera: Perlidae) and chironomid disturbances, providing greater opportunities for feeding, and larvae, Nanocladius (Plecopteracoluthus) sp., in the Neotropics. Studies on Neotropical Fauna and also eliminating metabolic waste. Ecologically, commensal life Environment, 35: 109-114. may still represent a largely vacant niche where the possibility of interspecific competition has been low (Tokeshi, 1993). Doucett, R.R.; Giberson, D.J. & Power, G. 1999. Parasitic association of Nanocladius (Diptera: Chironomidae) and Although, studies on the association between Chironomidae and Pteronarcys biloba (Plecoptera: Pteronarcyidae): insights other aquatic organisms have increased in the Neotropical from stable-isotope analysis. Journal of the North Region, mainly in Brazil, some questions still remain American Benthological Society, 18: 514-523. unanswered. More specific and detailed studies on these Dosdall, L.M. & Mason, P.G. 1981. A chironomid (Nanocladius associations are necessary. In the present study, we described (Plecopteracoluthus) branchicolus: Diptera) phoretic on a some of these associations. Some interactions are recorded for stonefly (Acroneuria lycorias: Plecoptera) in Saskatcherian. the first time for the state of Rio de Janeiro, such as those The Canadian Entomologist, 113: 141-147. between Aeshna punctata and Brechmorrhoga (Odonata), Dosdall, L.M. & Parker, D.W. 1998. First report of a Corydalus (Megaloptera), Grumicha grumicha (Trichoptera), symphoretic association between Nanocladius branchicolus and Trichomycterus mirissumba and Pareiorhina rudolphi Saether (Diptera: Chironomidae) and Argia moesta (Hagen) (Pisces). These results indicate that more detailed investigations (Odonata: Coenagrionidae). The American Midland might reveal new associations. Naturalist 139: 181-185.

17 Henriques-Oliveira & Nessimian

Epler, J.H. 1986. A novel new neotropical Nanocladius Moor, F.C. 1999. Phoretic association of blackflies (Diptera: (Diptera: Chironomidae) symphoretic on Traverella Simuliidae) with heptageniid mayflies (Ephemeroptera: (Ephemeroptera: Leptophlebiidae). The Florida Entomo- Heptagenidae) in South Africa. Africa Entomology, 7 (1): logist, 69: 319-327. 154-156. Epler, J.H. 1995. Identification manual for the larvae Pennuto, C.M.; Waster-Brow, C.L. & Belisle, C.A. 2002. Chironomidae (Diptera) of Florida. Departament of Infestation intensity and prevalence of an ectosymbiotic Environmental Protection. Division of Water Facilities, midge under variable environmental and host conditions. Tallahasse, VI + 308p. Canadian Journal of Zoology, 80: 2061-2071. Epler, J.H. & De La Rosa, C.L. 1995. Tempisquitoneura, a new Pennuto, C.M. 2003. Population dynamics and intraspecific genus of Neotropical Orthocladiinae (Diptera: Chironomidae) interactions of an ectosymbiotic midge in a river in southern symphoretic on Corydalus (Megaloptera: Corydalidae). Maine, USA. Journal of the North American Bentho- Journal North American Benthological Society, 14: 50-60. logical Society, 22: 249-262. Ferreira-Peruquetti, P. & Trivinho-Strixino, S. 2003. Relação Pepinelli, M.; Siqueira, T.; Salles, F.F. & Shimbori, E.M. 2009. forética entre espécies de Chironomidae e Odonata do Estado First report of Simuliidae and Chironomidae (Diptera) living de São Paulo. Entomotropica, 18: 149-151. on nymphs of Lachlania Hagen (Ephemeroptera: Fittkau, E.J. 1974. Ichthyocladius n. gen., eine neotropische Oligoneuriidae) in South America. 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Biota Neotropica, 4 -http://www. 1283-1294. biotaneotropica.org.br/v4n2/pt/abstract?short- communication+bn 03404022004 Giberson, D.J.; Macinnis, A.J. & Blanchard, M. 1996. Seasonal frequency and positioning of parasitic midges (Chironomidae) Rosa, B.F.J.V.; Martins, R.T.; Oliveira, V.C. & Alves, R.G. on Pteronarcys biloba nymphs (Plecoptera: Perlidae). Journal 2009. Phoretic associations between larvae of Rheotanytarsus North American Benthological Society, 15: 529-536. (Diptera: Chironomidae) and genera of Odonata in a first- order stream in an area of Atlantic Forest in Southeastern Hawking, J.H. & Watson, A.L. 1990. First australian record of Brazil. Zoologia, 26 (4): 787-791. chironomid larvae epizoic on larval Odonata. Aquatic Insects, 12: 241-245. Segura, M.O.; Fonseca-Gessner, A.A. & Batista, T.C. 2007. Associação forética entre larvas de Rheotanytarsus Hayashi, F. 1988. Life-history variation in a dobsonfly, (Chironomidae, Tanytarsini) e adultos de Elmidae (Coleoptera), Protohermes grandis (Megaloptera, Corydalidae) – effects of coletados em córregos no Parque Estadual de Campos de Jordão, prey availability and temperature. Freshwater Biology, 19: São Paulo, Brasil. Revista Brasileira de Zoologia, 24: 503-504. 205-216. Svensson, B.S. 1980. The effect of host density on the success Hayashi, F. 1998. Nanocladius (Plecopteracoluthus) asiaticus of commensalistic Epoicocladius flavens (Chironomidae) in sp. n. (Diptera: Chironomidae) phoretic on dobsonfly and utilizing stream living Ephemera danica (Ephemeroptera). fishfly larvae (Megaloptera: Corydalidae). Aquatic Insects, Oikos, 34: 326-336. 20: 215-229. Steffan, A.W. 1965. Plecopteracoluthus downesi gen. et sp. nov. Jacobsen, R.E. 1998. 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Freshwater Biology, 29: 481-489. News, 90: 33-36. Tracy, B.H. & Hazelwood, D.H. 1983. The phoretic association Mendes, H.; Andersen, T. & Saether, O. 2004. New species of of Urnatella gracilis (Entoprocta: Urnatellidae) and Ichthyocladius Fittkau, a member of the Corynoneura-group Nanocladius downesi (Diptera: Chironomidae) on Corydalus (Diptera: Chironomidae: Orthocladiinae), with a review of cornutus (Megaloptera: Corydalidae). Freshwater Inver- the genus. Studies on Neotropical Fauna and tebrate Biology, 2: 186-191. Environmental, 39: 15-35. White, T.R. & Fox, R.C. 1979. Chironomid (Diptera) larvae and Mendes, H.F.; Andersen, T. & Pinho, L.C. 2007. The female hydroptilid (Trichoptera) pupae in a phoretic relationship on a of Ichthyocladius kronichticola Mendes, Andersen & Sæther, macromiid (Odonata) nymph. Notulae Odonatologica, 1: 76-77. 2004 (Diptera: Chironomidae: Orthocladiinae). 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18 Lundiana 10(1):19-52, 2009 © 2011 Instituto de Ciências Biológicas - UFMG ISSN 1676-6180 Diversidad de Trichinelloidea (Enoplea, Nematoda) en Chile y su implicancia en salud humana, animal y ecosistémica

Julio A. San Martín-Órdenes Escuela de Postgrado, Programa M. Cs. Mención Producción, Manejo y Conservación de Recursos Naturales, Universidad de Los Lagos, Osorno, Chile. E-mail: [email protected]

Abstract Diversity of Trichinelloidea (Enoplea, Nematoda) in Chile and its implication for human, animal and ecosystemic health. The nematode zooparasites of vertebrate and invertebrate correspond to an aspect of biodiversity which has not been properly evaluated. In Chile, specific research on Trichinelloidea (Order Trichinellida) is scarce. For this reason, a recompilation on the taxa observed in this country was carried out, by means of a bibliographic review. The reported families are Capillariidae Néveu-Lemaire, 1936, with 11 identified species in Mammalia, Aves and Osteichtyes (including Capillaria sp. s. l. in Milvago chimango from the Metropolitan region, recorde here for the first time); Trichinellidae Ward, 1907, with one identified species in Mammalia; Trichuridae Railliet, 1915 with 11 species in Mammalia; and Trichosomoididae Hall, 1916; with one species in Rodentia. There were no records of these parasites associated with Reptilia, Amphibia, Agnatha, Chondrichtyes or to invertebrates, which are hosts recorded for the superfamily in other parts of the world. Involvement of species in this superfamily with human and ecosystemic health is argued, in the context of a debatable and confused taxonomy and identification, together with a scarce knowledge of this group. Therefore, it is considered that more studies on Trichinelloidea and its presence in this country are required.

Keywords: Parasites, Chile, Trichinelloidea, Capillaria, Trichinella, Trichuris, Trichosomoides, animal health, human health, ecosystem health.

Introducción Schmid-Hempel & Frank, 2007; Thompson et al., 2008). Por otra parte, los parásitos poseen una belleza intrínseca en su Los nemátodos zooparásitos de vertebrados e invertebrados apariencia o en sus ciclos de vida especialmente complejos que conforman un aspecto de la biodiversidad que no ha sido demuestran la “armonía” de la coevolución (Daszak & evaluado en detalle y que es importante desde el punto de vista Cunningham, 2002). De este modo no hay razón ética para no de la parasitología y también para aumentar el conocimiento de conservar la biodiversidad parasitaria de la misma forma que la las especies de vida libre con las que interactúan (Pérez-Ponce del hospedador (Daszak & Cunningham, 2002). de León & García, 2001). No obstante, actualmente, se han En Chile, los estudios sobre parásitos de diferentes grupos hecho algunos esfuerzos en el conocimiento de algunas especies taxonómicos son escasos, restringiéndose principalmente a de nemátodos (e.g. Viney, 2006; Schmid-Hempel & Frank, animales domésticos (Tagle, 1966; Tagle, 1970; Alcaíno & 2007). La situación anterior, tiene implicancias con respecto a la Gorman, 1999) y al hombre (Atías, 1991), aunque recientemente conservación parasitaria, la que a su vez, tiene ventajas prácticas se han realizado esfuerzos en la recopilación de datos en para la conservación de los hospedadores (Cunningham, 1996). animales silvestres (Puga, 1994; Cattán, 1995; Hinojosa-Sáez & El conocimiento de la biología y ecología evolutiva, asociada a González-Acuña, 2005; Olmos & Muñoz, 2006; Muñoz & la biodiversidad genética parasitaria puede entregar antecedentes Olmos, 2008). Precisamente, sobre la superfamilia sobre los ciclos y las asociaciones de hospedadores y parásitos, Trichinelloidea Ward, 1907 (Trichinellida Hall, 1916: Nematoda el desarrollo de inmunidad, los mecanismos de infección, Potts, 1932), no se han hecho muchos estudios específicos, virulencia y dosis infecciosa, que pueden ser útiles para el exceptuando en lo referente a Trichinella spiralis, especie sobre control de estos organismos (Viney, 2006, Gardner et al., 2007; la cual existe abundante información en el hombre, especies domésticas y sinantrópicas (Alcaíno & Arenas, 1981; Atías, 1991; Schenone et al., 1999). Received: 12-IX-07 La taxonomía de esta superfamilia ha sido muy discutida, Accepted: 10-I-09 incluyendo, de acuerdo a varios autores (Blaxter et al., 1998; Distributed: 13-IX-11 Moravec, 2001; De Ley & Blaxter, 2002), las familias

19 San Martín-Órdenes

Capillariidae, Trichinellidae, Trichuridae, Trichosomoididae, encontrado trabajos sobre la helmintofauna de especies parásitas Anatrichosomatidae, Cystoopsidae y Dioctowittidae. de Reptilia, Amphibia, Condrichtyes o Agnata ni tampoco en El trabajo presentado tiene como objetivo entregar una invertebrados, que involucren a esta superfamilia de nemátodos. recopilación de antecedentes de la superfamilia Trichinelloidea De las familias de Trichinelloidea, sólo cuatro (Capillariidae, con respecto a los parásitos descubiertos o recolectados en Trichinellidae, Trichuridae y Trichosomoididae) han sido Chile, para dimensionar, de manera más integral, los alcances de registradas dentro del país. este taxón en este país en el contexto de la biodiversidad De las especies de la familia Capillariidae se registran los parasitaria nacional. géneros Capillaria Zeder, 1800 con tres especies identificadas en Aves (C. columbae, C collaris y C. tenuissima), una especie Materiales y métodos de Baruscapillaria Moravec, 1982 en Aves (B. obsignata), una especie de Pterothominx Freitas, 1959 en Aves (P. caudinflata), Este trabajo es principalmente una revisión de literatura, tres de Eucoleus Dujardin, 1845 en Mammalia (E. aerophilus) y realizada a través de los portales buscadores Google Académico en Aves (E. annulatus y E. contortus), una de Calodium (http://scholar.google.cl); Scielo, la Biblioteca en línea Dujardin, 1845 en Mammalia (Calodium hepaticum), una de Electrónica Científica (http://www.scielo.cl/), Biblioteca Virtual Aonchoteca López-Neyra, 1947 en Mammalia (A. bovis) y una em Saúde (BVS), que incluye LILACS y Medline (http:// de Pearsonema Freitas & Mendonça, 1960 en Mammalia (P. bases.bvsalud.org); PubMed, desarrollado por el Center for plica). Además, se recopilaron Capillaria s.l. sp. en 26 taxa Biotechnology Information (NCBI) en el National Library of (especies o subespecies) de hospedadores (Tablas 2a-c). En Medicine (NLM) (http://www.ncbi.nlm.nih.gov/pubmed/) y Trichinellidae, se identificó una especie de Trichinella Railliet, Agris Caris, el sistema de información internacional para las 1895 (T. spiralis s. l.) en Mammalia (Tabla 2d) En Trichuridae, Ciencias y Tecnologías Agrícolas de la FAO (http:// se recopilaron 11 especies de Trichuris Roederer, 1761 en www.fao.org/agris/). De manera anexa, se revisó las bibliotecas Mammalia (T. bradleyi, T. chilensis, T. discolor, T. fulvis, T. digitales y sus tesis, de la Universidad de Concepción myocastoris; T. ovis, T. robustis; T skrjabini, T. suis, T. (www.bibliodigital.udec.cl), Universidad Austral de Chile (http:/ trichiura y T. vulpis), y 17 especies (o subespecies) de /cybertesis.uach.cl/), y Universidad Católica de Temuco (http:// hospedadores con registros sin identificar la especie de Trichuris www.uctem.cl/biblioteca/tesis.php), considerando su (Tablas 2d-g). En Trichosomoididae, se recopiló una especie de importancia en la investigación parasitológica en pregrado. Se Trichosomoides Railliet, 1895 en Rodentia (Mammalia) (T. incluye, también, los trabajos recopilatorios de Tagle (1966), crassicauda) (Tabla 2d). Para el caso del ave necropsiada, se Cattán (1995) y Alcaíno & Gorman (1999). Además, se ha agrega Capillaria sp. s.l, ya que algunos especimenes fueron agregado un registro nuevo de Capillaria sensu lato que fue obtenidos del intestino y se visualizaron nemátodos, obtenido durante la realización de mi tesis de Medicina aparentemente Trichinelloidea, en los cortes histológicos. Veterinaria. Para ello se utilizó la técnica de necropsia parasitaria descrita posteriormente por González-Acuña et al. (1) Trichinelloidea en hospedadores Mammalia Linnaeus, (2004a), en un tiuque [Milvago chimango chimango (Vieillot, 1758 1816), Falconidae, Aves] proveniente de la región El registro de Trichinelloidea en mamíferos chilenos se Metropolitana. El ave fue conservada mediante congelación y concentra en especies domésticas o sinantrópicas, incluyendo posteriormente, se les realizó cortes histológicos de acuerdo a gamos (Dama dama) y muflones (Ovis musimon) introducidos las técnicas estándares (Luna, 1968). (Díaz et al., 1977). Además, se agregan registros de roedores La nomenclatura utilizada para los taxones de Nematoda silvestres (Cattán, 1995; Landaeta-Aqueveque et al.; 2007), hasta el nivel de familia, corresponde a las de Blaxter et al. zorro chilla (Pseudalopex griseus) (Alarcón, 2005), guanaco (1998) y Moravec (2001). Para la familia Capillariidae, se utiliza (Lama guanicoe) (Henning, 1984) y pudú (Pudu puda) la sistemática de Moravec (1982) (Tabla 1), que es aceptada por (Valverde, 1988; Duval, 1990), dejando sin investigar, una gran la mayoría de los autores, actualmente (Okulewicz & Zalezny, cantidad de especies de mamíferos autóctonos no introducidos ni 2005). Se describe los helmintos Trichinelloidea bajo cinco asilvestrados que en total son 147 especies en la totalidad del apartados: (1) Trichinelloidea en hospedadores Mammalia territorio tricontinental (Contreras & Yáñez, 1995) (Tabla 3a y Linnaeus, 1758. (2) Trichinelloidea en hospedadores Aves 3b). Linnaeus, 1758. (3) Trichinelloidea en hospedadores Reptilia Laurenti, 1768 y Amphibia Linnaeus, 1758. (4) Trichinelloidea Capillariidae Néveu-Lemaire, 1936. Mundialmente incluye en hospedadores Pisces Linnaeus, 1758. y (5) Trichinelloidea en unas 300 especies de helmintos, que parasitan todos los grupos hospedadores invertebrados. Finalmente se discute sus de vertebrados (Okulewicz & Zalesny, 2005). Su desarrollo implicancias en la salud de animales y del ser humano, puede incluir oligoquetos o peces como hospedadores incluyendo aspectos zoonóticos de los parásitos y aquellos paraténicos (ciclos homoxenos) o intermedios (ciclos relacionados a la medicina de la conservación. heteroxenos) y sufren cuatro mudas durante su desarrollo ontogénico, el primero dentro del cuerpo del hospedador Resultados intermedio, en el caso de ciclos heteroxenos (Moravec et al., 1987). De los Capillariidae recolectados de mamíferos, a La recopilación de información sobre Trichinelloidea en continuación se registran sólo cuatro especies y el resto Chile tiene como resultado que sólo en individuos de especies de corresponde a registros de Capillaria sp. s. l. tres clases de vertebrados (Mammalia, Aves y Osteichthyes) se Aonchoteca bovis (Schnyder, 1906) Moravec, 1982 [sin. han hallado especimenes de este grupo de parásitos. No se han Capillaria bovis (Schnyder, 1906) Freitas & Lent, 1936; C.

20 Diversidad de Trichinelloidea en Chile

Tabla 1 - Distribución de géneros de Trichinelloidea en varias clases de hospedadores vertebrados basado en Moravec (1982) y complementado por Yamaguti (1961), Jones (1978), Moravec & Cosgrove (1982), Mas-Coma & Esteban (1985), Spencer-Jones & Gibson (1985), Baruš & Sergeeva (1990 a y c), Moravec & Spratt (1998), Gibson (2004), Justine (2005) y Pozio (2005). La lista incluye géneros que contienen una sp. inq (*) y una sp. incertae sedis (§).

Género Pisces Amphibia Reptilia Aves Mammalia Amphibiocapillaria Moravec, 1982 - + - - - Anatrichosoma Smith et Chitwood, 1954 - - - - + Aonchotheca López-Neyra, 1947 - + - + + Baruscapillaria Moravec, 1982 - - - + + Brevithominx Travassos, Freitas et Mendonça, 1964 - - - + - Calodium Dujardin, 1845 - - - - + Capillaria Zeder, 1800 + + + + + Capillostrongyloides Freitas et Lent, 1935 + - - - - Crocodylocapillaria Moravec et Spratt, 1998 - - + - - Cystoopsis Wagner, 1867 + - - - - Dioctowittus Chabaud et Le Van Hoa, 1968 - - + - - Echinocoleus López-Neyra, 1947 - - - + + Eucoleus Dujardin, 1845 - - - + + Freitascapillaria Moravec, 1982 + - - - - Gessyella Freitas, 1959 + - - - - Huffmanela Moravec, 1987 + - - - - Liniscus Dujardin, 1845 - - - - + Nematoideum Diesing 1851* - - - - + Ornithocapillaria Baruš et Sergeeva, 1990a - - - + - Paracapillaria Mendonça. 1963 + + + - - Paracapillaroides Moravec et al., 1999 + - - - - Paratrichosoma Ashford et Muller, 1978 - - + - - Pearsonema Freitas et Mendonça, 1960 - - - - + Piscicapillaria Moravec, 1982 + - - - - Pseudocapillaria Freitas, 1959 + - + + + Pseudocapillaroides Moravec et Cosgrove, 1982 - + - - - Pterothominx Freitas, 1959 - - - + + Schulmanela Ivashkin, 1964 + - - - - Tenoranema Mas-Coma et Esteban 1985 - - - - + Trichinella Railliet, 1895 - - + + + Trichosoma Rudolphi, 1819 *§ - + - - - Trichosomoides Railliet, 1895 - - - - + Trichuris Roederer, 1761 - - - - + Trichuroides Ricci, 1949 - - - - + Tridentocapillaria Baruš et Sergeeva, 1990c - - - + -

21 San Martín-Órdenes (1974a); San Martín- Baro (2000) (1974b) et al. (1976) al. (1974a); Cattán (1995) RBB, Chillán 36º36’ 72º02’ González-Acuña et al. (2004b) RR, Valdivia 39º48’ 73º12’ Torres & González (1972); I S RBB, Chillán 36º36’ 72º02’ González-Acuña et al. (2000) I D RR, Valdivia 39º48’ 73º12’ Torres (1971); et al. I D RR, Valdivia 39º48’ 73º12’ Torres et al. (1972) I D RR, RL ND ND Gómez (2000) I D Varios ND ND Boehmwald et al. (1971); Torres I Sa RM, Santiago 33º 7’ 70º 42’ Rojas et al. (1971) I D ND ND ND Tagle (1970) Phasianidae, AVESTinamidae, AVES I N D RR, Valdivia S 39º48’ RBB, Ñuble 73º12’ Torres et al. (1974b) Rubilar et al. (1996) Columbidae, AVESOdontophoridae, I S RBB, Chillán 36º36’ 72º02’ González-Acuña et al. (2004b) Phasianidae, AVESCanidae, I D RR, Valdivia 39º48’ 73º12’ Torres et al. (1974b) Columbidae, AVESPhasianidae, AVES I I S D RM, Santiago 33º 7’ RR, ValdiviaColumbidae, AVES 70º 42’ 39º48’ Toro et al. (1999) I 73º12’ González et al. (1974); Torres As RM, SantiagoFelidae, 33º 7’ 70º 42’ Toro et al. (1999) Bovidae, Falconidae, AVESCanidae, N S RBB, Chillán 36º36’ 72º02’ San Martín et al. (2006) Muridae, Phasianidae, AVES I D ND ND ND (1966) Tagle Bovidae, AVES MAMMALIA MAMMALIA MAMMALIA MAMMALIA MAMMALIA MAMMALIA y Columbidae, AVES I As RM, Santiago 33º 7’ 70º 42’ Toro et al. (1999) Gallus g. domesticus Nothoprocta perdicaria Columba livia Callipepla californica domesticus Columba livia Columba livia Gallus g. domesticus Felis catus Bos taurus Canis familiaris Milvago c. chimango Rattus norvegicus otros roedores Gallus g. domesticus

- Especies de Trichinelloidea en Chile.Capillariidae identificados. Especie Hospedador CLASE Familia, Origen Hábitat Localidad S W Cita Pearsonema plica Canis familiaris Pterothominx ata caudinfl Eucoleus annulatus Columba livia Eucoleus contortus Gallus g. Eucoleus aerophilus Capillaria tenuissima Capillaria columbae Baruscapillaria obsignata Calodium hepaticum Capillaria collaris Aonchoteca bovis Ovis aries Tabla 2a

22 Diversidad de Trichinelloidea en Chile (2007) (1995) (1998) (1986) (1986) Moreno (1981); Díaz et al. (1995b); Gutiérrez (2007) (1995) ND ND Landaeta-Aqueveque et al. ND ND Díaz et al. (1977) ND NDND Díaz et al. (1977) ND ND Miqueles & Gallo (1986) ND Henning (1984) 51º 30’ 73º 00’ Alarcón (2005) (p ) Santiago RM, SantiagoRupanco 33º 7’ 70º 42’ Salas (1985); Gorman et al. Parinacota Paine RM, Santiago 33º 7’ 70º 42’ Salas (1985); Gorman et al. RR, ValdiviaEsperanza 39º48’ 73º12’ Aguirre (2006) RARR, ValdiviaRMag, Magallanes NDRupanco 39º48’ 73º12’ ND ND Barlow, 1993 Jara (2001); Nitor (2006) ND Godoy (2002); Haustein (2003) y otros) I Sa RR, Valdivia 39º48’ 73º12’ Torres et al. (1976). I C RL, Isla Mayor L. I D RT, Pica 19º 51’ 69º 02’ Barraza (1998) N S RM, suburbios de N D RR, ValdiviaNN 39º48’ S 73º12’ C Sur de Chile Leiva (1997); Valenzuela et al. RM, Santiago ND ND ND ND Valverde (1988); Duval (1990) (1992) Wartluft N D RT (antigua), N S/C RMag, Torres del p (Capillariidae) no identificadas en Mamíferos de Chile. sensu lato

Capillaria ?, MAMMALIA N S ND ? ? Cattán (no publicado) en Muridae, MAMMALIA Cervidae, MAMMALIA Muridae, MAMMALIA Felidae, MAMMALIA I D RBB, Chillán 36º36’ 72º02’ Díaz et al. (1995a); López Canidae, MAMMALIA N S RMag, Última Bovidae, MAMMALIABovidae, Bovidae, Mammalia I D I RR, RLMAMMALIABovidae, D I RBB, Chillán C ND 36º36’ RL, Isla Mayor L. 72º02’ ND Burgos (1980) Gómez (2001) Camelidae, MAMMALIA Cervidae, MAMMALIA Canidae, MAMMALIA I D RBB, Ñuble (Chillán Camelidae, MAMMALIA Camelidae, MAMMALIA Camelidae, MAMMALIA roedores silvestres Rattus norvegicus Dama dama Abrothrix olivaceus Felis catus Pseudalopex griseus Bos taurus Ovis aries Ovis musimon Lama pacos Pudu puda Canis familiaris Lama glama Lama spp Lama guanicoe p sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. - Especies de Trichinelloidea en Chile. Especie Hospedador CLASE Familia, Origen Hábitat Localidad S W Cita Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Tabla 2b

23 San Martín-Órdenes (2004b) (2004); Araya (2005) ND Salinas et al. (2008) 73º 12’ CONAMA & UACH 73º 24’ Torres et al. (1993) S 39º 42’ 55’ - 33° 41º29 72º58’ Sepúlveda et al. (2004) co Suroeste 24° S RL, L. YelchoRR, Estuario R. ValdiviaRL, L. Llanquihue 39º52’RA, L. Caburga 73º20’ 43º16’RL, L. Yelcho Torreset al. (1982) 72º15’ 41º04’ Torres et al. (1992) 72º48’ 39º06’RL, L. Puyehue Torres et al. (1993) 71º45’ 43º16’ Torres et al. (1993) 72º15’ Torres et al. (1992) 40º36’ 73º44’ Torres et al. (1993) Juan Isla Guar, cerca de Puerto Montt I As RBB, Chillán 36º36’ 72º02’ González-Acuña et al. N S RR, Estuario R. Valdivia 39º52’ 73º20’ Torres et al. (1982) N S RAnt, playa Antofagasta 23º24’ 70° 36’ Oliva et al. (1996) N S RR, Estuario sector San N S RL, Metrencue, Codigue e NN S Pacífi S RBB, Talcahuano ND ND Garcías et al. (2001) no identificadas en Aves y Peces de Chile. Capillaria sensu lato Falconidae, AVESLaridae, AVES N N S RM, Santiago S RL, L. Huillinco, Chiloé 42º38’ 33º 7’ 74º00’ 70º 42’Phasianidae, AVES Torres et al. (1991) Trabajo presente Tyrannidae, AVES I NPodicipedidae, AVES D S RR, Valdivia Provincia de Ñuble 39º48’ ND 73º12’ Torres et al. (1974) ND Reyes (2008) Columbidae, AVES Laridae, AVESAnatidae, AVES N N S RL, L. Llanquihue S RR, SN Carlos Anwandter 41º04’ 39º 72º48’ Torres et al. (1993) Paralichthyidae, PISCES Batrachoididae, PISCES Pinguipedidae, PISCES Macrouridae, PISCES Sciaenidae, PISCES Milvago c. chimango Larus dominicanus Gallus g. domesticus Elaenia albiceps chilensis Podiceps major Columba livia Larus maculipennis Cygnus melanocoriphus Paralichthys adspersus Prolatilus jugularis Nezumia pulchella Cilus gilberti Aphos porosus sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. - Especies de Trichinelloidea en Chile. Especie Hospedador CLASE Familia, Origen Hábitat Localidad S W Cita Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Capillaria sensu lato Tabla 2c

24 Diversidad de Trichinelloidea en Chile Babero & Cattán (1975); Cattán et al. (1976); Monje (1993) (1987) ND NDND Babero et al. (1975); ND ND Babero et al. (1976) ND Cattán et al. (1992) 52º48’ 71º20’ Nitor (2006) 22º25’ 68º15’ Babero & Murúa 42º05’ 73º56’44º40’ Babero et al. (1979) 74º50’ Babero et al. (1979) Quebrada de la Plata Fuego RM, Suburbios de Santiago Arenas de Atacama RAGI, Arch. Los Chonos de Chiloé I D Cosmopolita ND ND Varias N S RM, Lo Curro y N S RAt, San Pedro N S RL, Isla Grande Suidae, MAMMALIASuidae, MAMMALIA IHominidae, MAMMALIA IFelidae, MAMMALIA DCanidae, MAMMALIA ND As I RR, Futrono IMuridae, MAMMALIA D D I ND Cosmopolita NDOctodontidae, CosmopolitaMAMMALIA ND ND Sa ND García et al. (2005) Tagle (1966) RR, Valdivia ND ND ND 39º48’ Varias 73º12’ Varias Torres et al. (1976) Muridae, MAMMALIA NBovidae, MAMMALIA S I RMag, Tierra del D RMag, Punta Ctenomyidae, MAMMALIA Myocastoridae, MAMMALIA

Sus scrofa domesticus Rattus norvegicus Sus scrofa Homo sapiens Felis catus longipilis phillipiensis

- Especies de Trichinelloidea en Chile. Trichinellidae, Trichosomoididae y Trichuridae. EspecieTrichinellidae Ward, 1907 familiaris Trichinella spiralis Hospedador CLASE Familia, Canis OrigenTrichosomoididae Hall, 1916 HábitatTrichosomoides Localidadcrassicauda Trichuridae Railliet, 1915 Trichuris bradleyi S Octodon degus W Cita Trichuris chilensis Abrothrix Trichuris discolor Ovis aries Trichuris fulvis Ctenomys fulvus Trichuris myocastoris Myocastor coipus Tabla 2d

25 San Martín-Órdenes Burgos (1991); Alcaíno & Gorman (1999) (1990) Álvarez (1994) ND ND Vega (1971) ND ND Skewes (1995) RMag, Estancia Oasy Harbour RBB, ChillánRR, ValdiviaRMag,Punta Arenas 36º36’ 52º48’ 72º02’ ND 71º20’ Burgos (1980) Nitor (2006) ND Opitz (1977) RBB, San Fabián de Alico ND ND Palma (2008) Punta Arenas 52º48’ 71º20’ Nitor (2006) RR, ValdiviaSan Carlos, ÑubleRR,ribera río ValdiviaRBB, Chillán 39º48’ 36º25’ ND 73º12’ 71º57’ Loyola (1976); Rosales Chiang (1979) ND 36º36’ Torres et al. (1995) 72º02’ Avilés (1997) I S P.N. Vicente Pérez N S RT, Canchone 20º25’ 69º35’ Babero & Murúa Bovidae, MAMMALIA I D ND ND ND Tagle (1966) Bovidae, MAMMALIABovidae, MAMMALIA I I D D ND ND ND ND ND ND Tagle (1966) Tagle (1966) Camelidae, MAMMALIA N D RT (antigua) ? ? Alcaíno et al. (1991); Ctenomyidae, MAMMALIA Bovidae, MAMMALIA I D RBB, Chillán 36º36’ 72º02’ Burgos (1980) Suidae, MAMMALIA I D NDHominidae, MAMMALIA I ND D ND Cosmopolita Tagle (1966) ND ND Varias Suidae, MAMMALIA I C RBB, Chillán 36°34’ 72°06’ Campos (2007) p() Bos taurus Capra hircus Lama glama Ctenomys robusti Ovis aries domesticus Homo sapiens Sus scrofa

- Especies de Trichinelloidea en Chile. Trichuridae (continuación). Especie Hospedador CLASE Familia, Origen Hábitat Localidad S W Cita Trichuris ovis Ovis aries Trichuris robustis Trichuris skrjabini Trichuris suis Sus scrofa Trichuris trichiura Tabla 2e

26 Diversidad de Trichinelloidea en Chile Haustein (2003) (1994) (2000) et al. (1986) Valenzuela et al. (1998) NDND ND ND Gorman et al. (2006) ND Vega (1971) ND Jara (2001) RA, Padre Las CasasRA, Melipeuco 78º45’RR, ValdiviaRMag, Punta Arenas 72º35’ Hidalgo (2004) 52º48’ ND 71º20’ Nitor (2006) ND Mendoza (1993) Barrera (2004) RA, PitrufquénRMag, Estancia Entre Vientos RA 38º58’ 72º38’ Herrera (1998) ND ND Godoy (2002); RR, ValdiviaRR, Los LagosRM, Santiago 39º48’RM, Providencia, Quinta Normal, La Pintana 39º51’ 73º12’ San Martín Baro Magallanes 33º 7’ 72º50’ Sandoval (2003) 70º 42’ López et al. (2006) RBB, Chillán 36º36’ 72º02’ Moreno (1981); Oneto CC RM, Santiago RR, ValdiviaC 33º 7’ RM, Santiago 70º 42’ 39º48’ Salas (1985); Gorman 73º12’ 33º 7’ Leiva (1997); 70º 42’ Ruiz (2000) Bovidae, MAMMALIA I D RA, Melipeuco Barrera (2004) Bovidae, MAMMALIA I D RMag, Provincia de Canidae, MAMMALIA I D ND ND ND Tagle, 1966 Camelidae, MAMMALIA N S RT (antigua) ND ND Olave (1986) spp. Camelidae, MAMMALIA N D RT (antigua), Pica 19º 51’ 69º 02’ Barraza (1998) Bos taurus Ovis aries Canis familiaris L. pacos Lama p() sp. sp. sp. sp. - Especies de Trichinelloidea en Chile. Trichuridae (continuación). Especie HospedadorCLASEOrigen Familia, Hábitat Localidad S W Cita Trichuris Trichuris Trichuris Trichuris vulpis Trichuris Tabla 2f

27 San Martín-Órdenes L: Los Santuario de La (1986) et al. (1986); Ruiz (2000) et al. (1986); Ruiz (2000) Montecinos (1998) Wartluft (1992) RR, Valdivia 39º48’ 73º12’ Aguirre (2006) S RT (antigua) ND ND Olave (1986) C RM, SantiagoC RA, Temuco 33º 7’C 70º 42’ RM, Buin Salas (1985); Gorman 38º44’ 72º36’C González (1997) RM, Santiago 33º43 70º44’ Cortés (2006) 33º 7’ 70º 42’ Ruiz (2000) I C RV, Quilpué 33º07’ 31º14’ Barrios (2005) N S RA, Lonquimay 38º25’ 71º30’ Torres et al. (1976) N S RMau, Laguna del Maule ND ND et al.(1976) Torres N C RM, Buin 33º43 70º44’ Cortés (2007) : R: región; T: Tarapacá; Ant: Antofagasta; At: Atacama; M: Metropolitana; Mau: Maule; BB: Bío-Bío; A: Araucanía; Los Ríos, MAMMALIA MAMMALIA MAMMALIA MAMMALIA Camelidae, MAMMALIA NCervidae, MAMMALIA C N RM, SantiagoSuidae, MAMMALIA S RAGI, RN Río Simpson 33º 7’ I 45º25’ 70º 42’ Salas (1985); Gorman 72º41’ C Aldridge y Cosmopolita ND ND Concha (2007) Camelidae, MAMMALIA N C RT (antigua), Parinacota ND ND Miqueles & Gallo Cervidae, MAMMALIA N S Sur de Chile ND ND Valverde (1988); Suidae, MAMMALIA I N RA, Pitrufquén 38º58’ 72º38’ Herrera (1998) Canidae, MAMMALIA I D RBB, Provincia de Ñuble ND ND Gutiérrez (2007) Canidae, MAMMALIA N S RMag, Última Esperanza 51º 30’ S 73º 00’ Alarcón (2005) Ctenomyidae, Ctenomyidae, Myocastoridae, Cebidae, MAMMALIA I C RV, Quilpué 33º07’ 31º14’ Barrios (2005) Cercopithecidae, : As: asilvestrado; C: cautiverio/ crianza; D: doméstico; S: silvestre; Sa: sinantrópico; L: lago; RN: Reserva Nacional; SN: Hábitat Localidad Lama guanicoe Hippocamelus bisulcus Sus scrofa Pudu puda Lama glama Sus scrofa domestica Canis familiaris Pseudalopex griseus C. maulinus brunneus C. maulinus maulinus Myocastor coipus Cebus albifrons Papio hamadryas sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. sp. - Especies de Trichinelloidea en Chile. Trichuridae (continuación). : N: nativo; I: introducido. Especie Hospedador CLASE Familia, Origen Hábitat Localidad S W Cita Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Trichuris Naturaleza. ND: No determinado. Lagos; AGI: Aysén; Mag: Magallanes. Tabla 2g Origen

28 Diversidad de Trichinelloidea en Chile

TABLA 3a - Tabla resumen de hospedadores (Mammalia: Carnivora y Artiodactyla) parasitados por Trichinelloidea en Chile

HOSPEDADOR Trichinelloidea Citas MAMMALIA Carnivora

Perro, Canis lupus familiares L., 1758 Eucoleus aerophilus Tagle, 1966; Boehmwald et al. (1971), Torres Pearsonema plica ( 1971); Torres et al. ( 1974a), Moreno (1981); Capillaria sp. s. l Oneto (1994); Cattán (1995); Díaz et al. Trichinella spiralis s. l (1995b); San Martín- Baro (2000); Sandoval Trichuris vulpis (2003); Aguirre (2006); Gorman et al. (2006); López et al., 2006; Gutiérrez (2007)

Zorro chilla, Pseudalopex griseus (Gray, 1869) Capillaria sp. s. l. Alarcón (2005) Trichuris sp.

Gato, Felis silvestris catus L., 1758 Eucoleus aerophilus Torres et al. (1972); Díaz et al. (1995a); López Capillaria sp. s. l. et al. (1995) Trichinella spiralis s.l.

Artiodactyla

Buey, Bos taurus L., 1758 Aonchoteca bovis Tagle, 1966; Gómez (2000); Barrera (2004) Capillaria sp. sensu lato Trichuris ovis Trichuris sp.

Cabra, Capra aegagrus hircus (L., 1758) Trichuris ovis Tagle, 1966; Palma (2008)

Oveja, Ovis aries L., 1758 Aonchoteca bovis Tagle, 1966; 1970; Vega (1971); Burgos Capillaria sp. s.l. (1980); Mendoza (1993); Herrera (1998); Trichuris ovis (como T. ovis y T. Jara (2001); Godoy (2002); Haustein (2003); globulosa) Barrera (2004); Hidalgo (2004); Nitor (2006) Trichuris discolor Trichuris skrjabini Trichuris sp.

Mufl ón, Ovis aries musimon Pallas, 1762 Capillaria sp. s. l. Díaz et al., 1977

Alpaca, L. pacos (L., 1758) Capillaria sp. s. l. Olave (1986); Salas (1985); Gorman et al. Trichuris sp. (1986); Leiva (1997); Valenzuela .et al., (1998); Ruiz (2000)

Llama, Lama glama L., 1758 Capillaria sp. s.l. Miqueles & Gallo (1986); Olave (1986); Salas Trichuris ovis (1985); Gorman et al. (1986); Alcaíno et al., Trichuris sp. (1991); Burgos (1991); González (1997); Alcaíno & Gorman (1999); Ruiz (2000);

Guanaco, L. guanicoe (Müller, 1776) Capillaria sp. s. l. Henning (1984); Salas (1985); Gorman et al. Trichuris sp. (1986); Ruiz (2000); Cortés (2006)

29 San Martín-Órdenes

TABLA 3a - Tabla resumen de hospedadores (Mammalia: Carnivora y Artiodactyla) parasitados por Trichinelloidea en Chile (continuación).

HOSPEDADOR Trichinelloidea Citas MAMMALIA Carnivora

Gamo, Dama dama L., 1758 Capillaria sp. s. l. Díaz et al. (1977)

Huemul, Hippocamelus bisulcus (Molina, Trichuris sp. Aldridge y Montecinos (1998). 1782)

Pudú, Pudu puda (Molina, 1782) Capillaria sp. s.l. Valverde (1988); Duval (1990) Wartluft Trichuris sp. (1992); Ruiz (2000)

Cerdo, Sus scrofa domestica L., 1758 Trichinella spiralis s.l. Tagle (1966); Loyola (1976); Chiang (1978); Trichuris suis Álvarez (1994); Torres et al. (1995); Avilés Trichuris sp. (1997); Herrera (1998)

Jabalí, Sus scrofa L., 1758 Trichinella spiralis s.l. Skewes (1995); García et al. (2005); Campos Trichuris suis (2007); Concha (2007) Trichuris sp.

longipes Ransom, 1911], ha sido registrada, en una única (Bhalerao, 1933), A. brevipes (Ransom, 1911), [sinónimo de A. ocasión en ovejas de Chile, no especificando su origen (Tagle, bovis, Justine & Ferté (1988)] y A. megrelica (Rodonaja, 1947) 1970), pero como C. longipes, un sinónimo posterior (Justine & (López-Neyra, 1947; Yamaguti, 1961). También se describió la Ferté, 1988). También fue registrada como C. bovis en especie A. musimon Pisanu & Bain, 1999 de muflones en el necropsias de bovinos realizadas en la Universidad Austral de Archipiélago de Kerguelen en el Océano Índico (Pisanu & Bain, Chile (Gómez, 2000). Esta especie ha sido hallada en especies 1999). de Bovidae (Bos taurus, O. aries), Cervidae y Antilocapridae de Algo similar a lo que sucede con las especies de cérvidos, se Eurasia y América (López-Neyra, 1947; Yamaguti, 1961; puede inferir con respecto al hallazgo de huevos de Capillaria Prestwood et al., 1975). De este modo, los individuos de sp. s.l. en los Camelidae domésticos Lama pacos, de Valdivia Capillaria sp. s.l. hallados en los Bovidae, B. taurus en Valdivia (Leiva, 1997; Valenzuela et al., 1998) y de la región (Gómez, 2000); O. aries de las regiones del Biobío (Burgos, Metropolitana (Salas, 1985; Gorman et al.; 1986), L. glama, de 1980), La Araucanía (Godoy, 2002; Haustein, 2003) y la primera región (antigua) de Chile (Miqueles & Gallo, 1986; Magallanes (Jara, 2001; Nitor, 2006) y O. aries musimon en la Barraza, 1998) y con la especie silvestre, L. guanicoe, de isla Mayor del Lago Rupanco (Díaz et al., 1977), posiblemente ejemplares silvestres de Torres del Paine (Henning, 1984) y corresponden a esta especie. Además, los hallazgos en P. puda mantenidos en cautiverio (Salas, 1985; Gorman et al., 1986). silvestres del sur de Chile y mantenidos en cautiverio en la Eucoleus aerophilus (Creplin, 1839) Dujardin, 1845 [sin. región Metropolitana (Valverde, 1988; Duval, 1990; Wartluft, Capillaria (Thominx) aerophila (Creplin, 1839) Travassos, 1992) y D. dama, también de la isla Mayor (Díaz et al., 1977) 1915], ha sido descrita como parásito de perros y gatos de pueden atribuirse a la especie mencionada, porque los cérvidos Santiago y Valdivia (Boehmwald et al., 1971; Torres et al., son afectados frecuentemente por parásitos (incluyendo 1972; Torres et al., 1974a; Cattán, 1995). Esta especie está Capillaria sp.) de animales domésticos, especialmente bovinos ampliamente distribuida en países del hemisferio norte y (Maldonado, 1997). Australia, hospedada por estos carnívoros domésticos y además, Otras especies de Capillariidae que afectan al ganado y que de otros Carnivora e Insectivora (erizo de tierra, Erinaceus potencialmente afectarían a cérvidos del mundo son A. bilobata europeus) (Yamaguti, 1961; Holmes & Kelly, 1973).

30 Diversidad de Trichinelloidea en Chile

TABLA 3b - Tabla resumen de hospedadores (Mammalia: Primates y Rodentia) parasitados por Trichinelloidea en Chile.

HOSPEDADOR Trichinelloidea Citas MAMMALIA Primates

Capuchino de frente blanca, Cebus albifrons (Humboldt, Trichuris sp. Barrios (2005) 1812)

Papión sagrado, Papio hamadryas L., 1758 Trichuris sp. Barrios (2005)

Hombre, Homo sapiens sapiens L., 1758 Trichinella spiralis s.l. Varios Trichuris trichiura

Rodentia

Tuco-tuco, Ctenomys maulinus brunneus Osgood, 1943 Trichuris sp. Torres et al. (1976)

Tuco-tuco, Ctenomys maulinus maulinus Philippi, 1872 Trichuris sp. Torres et al. (1976)

Tuco-tuco, Ctenomys fulvus phillipiensis Trichuris fulvis Babero & Murúa (1987)

Tuco-tuco, Ctenomys robustus Philippi, 1896 Trichuris robustis Babero & Murúa (1990)

Rata o guarén, Rattus norvegicus Berkenhout, 1769 Calodium hepaticum Rojas et al. (1971); Torres & Capillaria sp. s. l. González (1972); Torres et al. (1976) Trichosomoides crassicauda

Ratón lanudo, Abrothrix longipilis (Waterhouse, 1837) Trichuris chilensis Babero et al (1976); Cattán et al. (1992)

Ratón oliváceo, Abrothrix olivaceus (Waterhouse, 1837) Capillaria sp. s. l. Landaeta-Aqueveque et al. (2007)

Degú, Octodon degus (Molina, 1782) Trichuris bradleyi Babero et al. (1975); Babero & Cattán (1975); Cattán et al. (1976); Monje (1993)

Coipo, Myocastor coipus (Molina, 1782) Trichuris myocastoris Babero et al. (1979); Cortés (2007) Trichuris sp.

Roedores silvestres Capillaria sp. s. l. Cattán (1995)

Pearsonema plica (Rudolphi, 1819) Moravec, 1982 [sin. Unidos (López-Neyra, 1947; Yamaguti, 1961). Se han registrado Capillaria plica (Rudolphi, 1819) Travassos, 1915], ha sido huevos de Capillaria sp. s.l. provenientes de perros y gatos de hospedada por perros y gatos de Valdivia (Torres, 1971, Torres localidades de la región del Biobío (Moreno, 1981; López, 1995; et al., 1974a; San Martín-Baro, 2000). Además, se ha obtenido Díaz et al. 1995a y b; Gutiérrez, 2007) y de Valdivia (Aguirre, de la vejiga urinaria de Canidae y Felidae de Europa y Estados 2006). Otras especies que afectan a Carnivora domésticos y

31 San Martín-Órdenes

TABLA 3c - Resumen de hospedadores (Aves y Pisces) parasitados por Trichinelloidea en Chile.

HOSPEDADOR Trichinelloidea Citas AVES

Cisne cuello negro, Cygnus melanocoriphus (Molina, 1782) Capillaria sp. s.l CONAMA Xª región de Los Lagos & UACH (2004); Araya (2005)

Codorniz, Callipepla californica (Shaw, 1798) Pterothominx caudinfl ata González-Acuña et al. (2000)

Fío-fío, Elaenia albiceps chilensis Hellmayr, 1927 Capillaria sp. s.l. Reyes (2008) (como Thominx sp.)

Gallina, Gallus g. domesticus (L., 1758) Baruscapillaria obsignata Tagle (1966); González Capillaria collaris et al. (1974); Torres et al. Eucoleus contortus (1974b) Pterothominx caudinfl ata Capillaria sp. s. l.

Gaviota cáhuil, Larus maculipennis Lichstenstein, 1823 Capillaria sp. s. l. Torres et al. (1992; 1993)

Gaviota dominicana, Larus dominicanus Lichstenstein, 1823 Capillaria sp. s. l. Torres et al. (1982; 1991; 1992; 1993)

Huala, Podiceps major (Boddaert, 1783) Capillaria sp. s. l. Torres et al. (1982)

Paloma, Columba livia (Gmelin, 1789) Baruscapillaria obsignata Toro et al. (1999); Capillaria columbae González-Acuña et al. Eucoleus annulatus (2004b) Pterothominx caudinfl ata Capillaria sp. s.l.

Perdiz chilena, Nothoprocta perdicaria (Kittlitz, 1830) Pterothominx caudinfl ata Rubilar et al. (1996)

Tiuque común, Milvago c. chimango (Vieillot, 1816) Capillaria tenuissima San MartÍn et al. (2006); Capillaria sp. s. l. trabajo presente

PISCES (OSTEICHTYES)

Bagre de mar, Aphos porosus (Schneider, 1801) Capillaria sp. s. l. Torres et al. (1993)

Blanquillo, Prolatilus jugularis (Valenciennes, 1833) Capillaria sp. s. l. Sepúlveda et al. (2004)

Corvina, Cilus gilberti (Abbott, 1899) Capillaria sp. s. l. Garcías et al. (1999)

Lenguado, Paralichthys adspersus (Steindachner, 1867) Capillaria sp. s. l. Oliva et al. (1996)

Pejerrata, Nezumia pulchella (Pequeño, 1971) Capillaria sp. s. l. Salinas et al. (2008)

32 Diversidad de Trichinelloidea en Chile

silvestres son Pearsonema feliscati (Belingham, 1840) Moravec, pesquizado en perros y gatos de la región Metropolitana 1982; Capillaria linearis (Leidy, 1856) sp. inq., Baruscapillaria (Alcaíno & Arenas, 1981; Alcaíno et al., 1981b; Gorman et al., pachykeramota (Wedl, 1856) Moravec, 1982 (Yamaguti, 1961; 1991). Oberg et al. (1979) diagnosticaron la triquinelosis en Moravec, 1982) y Aonchoteca putorii (Rudolphi, 1819) López- perros de la comuna de Máfil (Región de Los Ríos). Más Neyra, 1947 (Curtsinger et al., 1993). recientemente, mediante ELISA se halló Trichinella sp. en Calodium hepaticum (Bancroft, 1893) Moravec, 1982 [sin. perros de la localidad rural de Santa Clara (Ñuble, Región del Capillaria hepatica (Bancroft, 1893) Travassos, 1915], se Biobío) (Gatica, 2006). registró en Chile, a través del diagnóstico por hallazgo de También se han realizado investigaciones en mamíferos lesiones en hígados de ratas (R. norvegicus) de Santiago (Rojas salvajes (Álvarez et al., 1970; Alcaíno & Arenas, 1981; Cherres, et al., 1971), para posteriormente comprobarse la presencia de 2004) sin resultados positivos. La prevalencia de Trichinella helmintos de esta especie en roedores provenientes de Valdivia spiralis es baja y se ha constatado una disminución en casos (Torres & González, 1972; Torres et al., 1976). Esta especie humanos y cerdos, aunque varios miles de personas han sido también fue identificada en los Altos Andes de Perú en una afectadas (Schenone et al., 1997, Schenone et al., 2002). especie de cuy (Cavia aperea) (Dittmar, 2002). En roedores, también se agregan otros registros de Trichuridae Railliet, 1915. Comprende helmintos que Capillaria sp. (s. l.), provenientes del intestino delgado de habitan en el ciego, intestino grueso, cuyos ciclos son directos e Rattus norvegicus de Valdivia (Torres et al., 1976), en el involucran el consumo de huevos embrionados desde el suelo estómago de Abrothrix olivaceus (Landaeta-Aqueveque et al., (Georgi et al., 1990). Entre los Trichuridae de mamíferos; 2007) y en roedores silvestres (Cattán, 1995) que pueden Trichuris suis y T. trichiura a veces son consideradas especies corresponder a otra especie, existiendo una amplia variedad de sinónimas, pero según el criterio de Lanfredi et al. (1995), se ha Capillariidae que afectan a roedores (López-Neyra, 1947; demostrado que corresponden a especies diferentes. Yamaguti, 1961). Trichuris trichiura (Linnaeus, 1771) Stiles, 1901; ha sido registrada en Chile en varios estudios que muestran su presencia Trichinellidae Ward, 1907. De acuerdo a trabajos actuales y prevalencia en el ser humano, que se basan principalmente en (Pozio et al., 1992; Pozio et al., 1999; Pozio & La Rosa, 2000; exámenes coprológicos y algunos con especimenes adultos Pozio et al., 2002), está compuesta por varias especies del (Neghme & Silva, 1963; Bórquez et al., 2004; Martínez et al., género tipo Trichinella, que parasitan a más de 150 especies de 2006). Es una especie de distribución cosmopolita, descrita en el 12 órdenes de mamíferos, principalmente carnívoros o hombre y otros Primates (Yamaguti, 1961). Los hallazgos en carroñeros y al hombre; aunque se han descrito algunas especies Primates no humanos y exóticos del Zoológico de Quilpué de Trichinella en aves e incluso animales poiquilotermos (Región de Valparaiso) (Barrios, 2005), podrían corresponder a (Moravec, 2001; Pozio, 2005). Este amplio espectro de esta especie (Ooi et al., 1993). hospedadores y la presencia o ausencia de encapsulamiento en la Trichuris ovis (Abildgaard, 1795) Smith, 1908; ha sido etapa larvaria ha llegado a sugerir la división del género (Pozio hallada en ganado bovino, caprino y ovino (Tagle, 1966). Esta et al., 2001). Trichinellidae presenta un ciclo de vida único, especie se distribuye mundialmente y ha sido descrita en varias donde los vermes sufren su desarrollo completo en un único especies de Artyodactila (Yamaguti, 1961). En ovejas de Chile, hospedador vertebrado (autoheterogenia), con cinco etapas hay varios registros, como T. ovis y como T. globulosa, larvarias, localizadas en las células musculares esqueléticas del considerada sinónima de T. ovis por Cutillas et al. (1995); en la hospedador (Zarlenga et al., 2006). regiones del Biobío (Burgos, 1980), de Los Ríos (Opitz, 1977) y Trichinella spiralis (Owen, 1835) Railliet, 1895; especie en la de Magallanes (Vega, 1971; Nitor, 2006) y en cabras en asociada, casi exclusivamente al hábitat doméstico (Kapel, San Fabián de Alico (Región del Biobío) (Palma, 2008). 2000), en los ciclos domésticos (Pozio, 2000). En Chile, se ha Además, hay varios registros en ovinos de Trichuris sp. (Vega, comprobado la presencia de larvas de Trichinella sp. en la 1971; Mendoza, 1993; Herrera, 1998; Jara; 2001; Godoy, 2002; momia incaica del niño del cerro El Plomo (Valenzuela, 2005). Haustein, 2003; Barrera, 2004; Hidalgo, 2004; Nitor; 2006) en Ha sido registrada en humanos desde el siglo XIX (Cornejo, varias regiones y en B. taurus de Melipeuco (región de la 1883-1884; Poupin, 1897) y se continuaron diagnosticando Araucanía) (Barrera, 2004). También se ha encontrado Trichuris hallazgos durante el siglo XX, hasta la fecha en diversos lugares sp. en llamas y alpacas del Norte Grande de Chile (Miqueles & del país (Tagle, 1970; Alcaíno & Arenas, 1981; Schenone et al., Gallo, 1986; Olave, 1986; Alcaíno et al., 1991; Burgos, 1991; 1994; Schenone et al., 1997). Desde la primera mitad del siglo Barraza, 1998; Alcaíno & Gorman, 1999), Santiago (Salas, XX se ha llevado estudios de los animales afectados por este 1985; Gorman et al.,1986; Ruiz, 2000), Temuco (González, helminto, principalmente, el cerdo (Tagle, 1970; Alcaíno & 1997) y Valdivia (Leiva, 1997; Valenzuela et al., 1998) y en Arenas, 1981; Alcaíno et al., 1981a, Schenone et al., 1999) y a guanacos (L. guanicoe) mantenidos en cautiverio (Salas, 1985; roedores sinantrópicos que son hospedadores depredados Gorman et al., 1986; Ruiz, 2000; Cortés, 2006). muchas veces por los primeros (Tagle, 1970; Rojas et al., 1971; La mayoría de los hallazgos no identificados Trichuris han Alcaíno & Arenas, 1981). Además, en Chile, T. spiralis se sido realizados mediante examen coprológico. No se debe diagnosticó indirectamente en el jabalí, especie silvestre descartar otras especies descritas en camélidos y bóvidos en introducida, mediante el diagnóstico en un hombre proveniente otros países, como T. lama Ezzat, 1945; T. skrjabini Baskakow, de Futrono (Región de los Ríos), que había consumido su carne 1924; T. cameli (Rud. 1819), considerada sinónimo de T. (García et al., 2005). echinophallus (Nitzsch en Crepl., 1849) y de T. ovis; y T. tenuis Se han realizado estudios con el fin de conocer sus Chandler, 1930 (Yamaguti, 1961; Rickard & Bishop, 1991). implicancias dentro del medio antropizado, por lo que se ha Esta última especie que ha sido también descrita en guanacos de

33 San Martín-Órdenes

Argentina (Karesh et al. 1998; Beldomenico et al., 2003), por lo Trichuris fulvis Babero & Murúa, 1987 fue descrita del que es posible que esté presente en Chile. tuco-tuco de Atacama (Ctenomys fulvus phillipiensis) También en el huemul [H. bissulcus (Molina)] de la Reserva proveniente de San Pedro de Atacama (Babero & Murúa, 1987). Nacional Río Simpson (Región de Aysén) se halló, mediante Trichuris robustis Babero & Murúa, 1990 obtenida del examen coprológico, huevos de Trichuris sp. (Aldridge y tuco-tuco del tamarugal (Ctenomys robustus) proveniente de Montecinos, 1998). También se encontró Trichuris sp., Canchone, en la Provincia de Tarapacá (Babero & Murúa, coprológicamente en pudúes (P. puda) de la zona sur y 1990). También en algunos trabajos se han registrado algunos mantenidos en cautiverio en Santiago (Valverde, 1988; Wartluft, Trichuris no identificados en individuos de dos subespecies de 1992; Ruiz, 2000). En cuanto a especies de Trichuris obtenidas tuco-tuco (C. maulinus maulinus, Sector de Laguna del Maule y de cérvidos, Trichuris lani (Artiukh, 1948) y T. longispicula C. maulinus brunneus, sector de Lonquimay) (Torres et al., (Artiukh, 1948) son especies no registradas en el país, pero 1976). halladas en Cervus dama y Rangifer tarandus, respectivamente Trichuris myocastoris Enigk, 1933; fue registrado de coipos (Yamaguti, 1961), cérvidos que han sido introducidos en Chile (Myocastor coipus) capturados en la Región de los Lagos y en la para cotos de caza (Campos, 1996). Región de Aysén de Carlos Ibáñez del Campo (Babero et al., Trichuris discolor (von Linstow, 1906) Ransom, 1911, fue 1979), aparte de especimenes introducidos a Europa (Yamaguti, obtenida de ovejas beneficiadas en un matadero de Punta Arenas 1961). Cortés (2007) diagnosticó mediante coprología (Región de Magallanes) (Nitor, 2006). Parasita el ciego e parasitaria huevos de Trichuris sp. en coipos del Buin Zoo intestino grueso de vacas, ovejas, cabras y otros rumiantes (Región Metropolitana) que pueden corresponder a esta especie. provenientes de diferentes continentes (Hidalgo-Argüello & Cordero del Campillo, 1999). Trichosomoididae Hall, 1916 incluye especies que afectan Trichuris skrjabini Baskakov, 1924, fue obtenida de ovejas principalmente a mamíferos del orden Rodentia (género provenientes de la zona de Chillán (Burgos, 1980) y de Trichosomoides Railliet, 1895), (Yamaguti, 1961). El ciclo de Magallanes (Nitor, 2006). Es un parásito de varias especies Trichosomoides crassicauda es directo (Serakides et al., 2001). como camellos, ovinos, caprinos, bovinos y otros rumiantes y Trichosomoides crassicauda (Bellingham, 1845) Railliet, que ha sido aislado en Rusia y otros países de Europa, África, 1895; es la única especie registrada en Chile de Asia y América (Skrjabin et al., 1957; Knight, 1971; Martínez et Trichosomoididae, lo que fue realizado en la especie Rattus al. 1978; Reinecke et al., 1989; Hidalgo-Argüello & Cordero del norvegicus proveniente de Valdivia (Torres et al., 1976). Los Campillo, 1999). machos son parásitos de la vagina y útero de las hembras y Trichuris suis (Schrank, 1788) Smith, 1908; es parásito del habitan en la pelvis renal, uréteres vejiga urinaria de roedores de cerdo doméstico que fue diagnosticada en Chile por Tagle todo el mundo, siendo cosmopolita (López-Neyra, 1947; (1966), que no precisa su lugar de origen; en la zonas de Ñuble Yamaguti, 1961). Otras especies exóticas de este género son T. (Chiang, 1978; Avilés, 1997) y Valdivia (Loyola, 1976; nasalis Biocca & Aurizi, 1961 y T. spratti Diagne, Diouf, Álvarez, 1994; Torres et al., 1995). También ha sido registrado Lochouarn & Bain, 2000, que parasitan a roedores (Diagne et en jabalíes silvestres y en criaderos (Skewes, 1995; Campos, al., 2000). Trichuroides Ricci, 1949, es un género de 2007). También hay hallazgos de Trichuris sp. en cerdos Trichinelloidea descrito en Italia, que parasita la vejiga urinaria provenientes de Pitrufquén (Región de la Araucanía) (Herrera, de murciélagos y cuya taxonomía no está clara (genus 1998) y en jabalíes de criadero (Concha, 2007), que inquirendum), existiendo dudas sobre su ubicación dentro de probablemente correspondan a la misma especie. Trichuris suis Trichosomoididae (Gibson, 2004). es de distribución cosmopolita, al igual que su hospedador tipo (Yamaguti, 1961). Anatrichosomatidae Yamaguti, 1961; también Trichuris vulpis (Froelich, 1789) Smith, 1908; primero ha considerada la subfamilia Anatrichosomatinae Smith & sido registrado en perros en Chile por Tagle (1966), en Santiago Chitwood, 1954; familia Trichosomoididae York & (Gorman et al., 2006; López et al., 2006), Chillán (Moreno, Maplestone, 1926 (Moravec, 2001), afecta tejidos conectivos 1981; Oneto, 1994), Valdivia (San Martín- Baro, 2000) y Los de diversos mamíferos, y de transmisión y ciclo Lagos (Sandoval, 2003). También, existe un registro de desconocidos. Hasta la fecha, no hay registros de parásitos de Trichuris sp. en zorro chilla (P. griseus) proveniente de las familias Anatrichosomatidae en Chile. Esta familia Magallanes (Alarcón, 2005), que puede corresponder a la misma contiene las especies Anatrichosoma cutaneum (Swift, Boots especie, porque T. vulpis, ha sido recolectada de especies de & Miller, 1922) Smith & Chitwood, 1956; A. cynamolgi Canidae originarias de diversas partes del mundo (Yamaguti, Smith & Chitwood, 1954 (sin. A. rhina Conrad & Wong, 1961). 1973 y A. nacepobi Conrad & Wong, 1973; Long et al., Trichuris bradleyi Babero, Cattán & Cabello, 1975, 1976); que son parásitas de la mucosa nasal y cutis de especie obtenida desde el degú común (Octodon degus) Primates Macaca spp. (Conrad & Wong, 1973; Long et al., proveniente de los sector de Lo Curro y Quebrada de la Plata 1976; Kessler, 1982). Otras especies de Anatrichosomatinae (Región Metropolitana) (Babero et al., 1975; Babero & Cattán, son A. buccalis Pence & Litle, 1972 y A. haycocki Spratt, 1975; Cattán et al., 1976; Monje, 1993). 1982 que parasitan mucosas de Marsupialia (Pence & Litle, Trichuris chilensis Babero, Cattán & Cabello, 1976 fue 1972; Spratt, 1982); A. gerbillis (Bernard, 1964) (sin. obtenido desde el aparato digestivo del ratoncito lanudo Skrjabinocapillaria rodentium Wertheim & Chabaud, 1979), (Abrothrix longipilis) proveniente de Tierra del Fuego (Región del estómago de roedores (Spratt, 1982) y A. ocularis File, de Magallanes) (Babero et al., 1976) y de las cercanía de 1974 de la mucosa ocular del Scandentia Tupaia glis (File, Santiago (Cattán et al., 1992). 1974).

34 Diversidad de Trichinelloidea en Chile

(2) Trichinelloidea hospedados por Aves Linnaeus, 1758 de Galliformes y Columbiformes (domésticos y silvestres) En cuanto a aves chilenas, el registro de hospedadores (Baruš & Sergeeva, 1990a; Vicente et al., 1995) y raramente en también es estrecho, ya que abarca principalmente gallinas, Passeriformes, Anseriformes y Psittaciformes (Baruš & palomas, gaviotas y algunas aves de caza y de presa (Tabla 3c); Sergeeva, 1990a; Kajerová & Baruš, 2005). dejando fuera de estudio otras especies de aves de interés Pterothominx caudinflata (Molin, 1858) Okulewicz, 1993 productivo y aves sin interés cinegético, pero incluidas dentro de [sin. Capillaria caudinflata (Molin, 1858) Wawilowa, 1926; las 380 especies que son estables en nuestra ornitofauna y en Aonchotheca caudinflata (Molin, 1858) Moravec, 1982]; es una cerca de 80 accidentales (Jacksic, 1997), que son potenciales especie polixena que ha sido encontrada en gallinas de la zona hospedadores. Aparte de Capillariidae, no se han hallado otros de Valdivia (Torres et al., 1974b); en el duodeno-íleón de perdiz Trichinelloidea en aves de Chile. chilena de Ñuble (Rubilar et al., 1996), codorniz californiana de Ñuble (González-Acuña et al., 2000) y en palomas asilvestradas Capillariidae Néveu-Lemaire, 1936. Incluye gran parte de de Chillán (González-Acuña et al., 2004b). Mundialmente, se ha especimenes de Capillaria s.l. no identificados hasta el nivel de obtenido del intestino de especies de aves Columbidae, especie. Las especies parásitas de aves identificadas en Chile Strigidae, Passeriformes y Galliformes de Europa y son: Norteamérica (Yamaguti, 1961), en intestino delgado de gallinas Capillaria collaris (Linstow, 1873) Skrjabin & domésticas de Brasil (Vicente et al., 1995) y además, hay un Shikhobalova, 1954 [sin. C. retusa (Railliet, 1893) Travassos, registro excepcional en el cernícalo común europeo (F. 1915]; sólo se ha registrado en Chile una única vez en la gallina tinnunculus) de Países Bajos (Borgsteede et al., 2003). doméstica (Tagle, 1966) y mediante la nomenclatura sinónima y Eucoleus contortus (Creplin, 1839) Gagarin, 1951 [sin. posterior, C. retusa (Freitas & Almeida, 1935; Gassal, 2003). Capillaria contorta (Creplin, 1839) Travassos, 1915]; es un Esta especie ha sido registrada de diferentes Galliformes de helminto polixeno que habita la mucosa del esófago, cavidad Eurasia, y América (Yamaguti, 1961), incluyendo Brasil de oral y excepcionalmente el estómago glandular de una gran donde se ha obtenido, además, de Anseriformes domésticos cantidad de hospedadores de diferentes órdenes, tales como (Vicente et al., 1995). Anseriformes, Passeriformes, Columbiformes, Charadriiformes Capillaria columbae (Madsen, 1945) Graybill, 1924; ha y otras aves de Europa, América del Norte y del Sur, y Asia sido hallada en palomas asilvestradas (Columba livia) de (Yamaguti, 1961. Vicente et al., 1995, Betlejewska et al., 2002). Santiago (región Metropolitana) (Toro et al., 1999) y de Chillán En Chile, existe un registro en gallina doméstica proveniente de (región del Biobío) (González-Acuña et al., 2004b). Es una Valdivia (Torres et al., 1974b) que posiblemente constituya una especie cosmopolita que también ha sido obtenida de palomas mala identificación. De acuerdo a Baruš & Sergeeva (1989) y asilvestradas y Galliformes del mundo (Yamaguti, 1961), y Moravec (1982) todos los Capillariidae encontrados en el tracto también del tucán grande (Ramphastos toco, Piciformes) de digestivo anterior de aves terrestres incluyendo E. contortus, Brasil (Vicente et al., 1995). deben ser relacionadas a E. dispar u otra especie de Eucoleus, ya Capillaria tenuissima (Rudolphi, 1809) Yamaguti, 1941; que E. contortus parasita a aves acuáticas. Esto se puede ha sido recolectada de los estómagos e intestinos de tiuques relacionar a que algunos autores consideran los hallazgos de (Milvago chimango chimango) de Chillán (Región del Biobío) estas especies diferentes como sinónimos (Ferrer et al., 2004; (San Martín et al., 2006). Los especimenes de Capillaria sp. s. l Sanmartín et al., 2004). encontrados en el intestino de tiuque común, proveniente de Eucoleus annulatus (Molin, 1858) López-Neyra, 1947 Santiago, y reportados en este trabajo, podrían corresponder a [Capillaria annulata (Molin, 1858) Cram, 1926]; fue esta especie. Capillaria tenuissima ha sido registrada en varias recolectada de palomas asilvestradas de Santiago (Toro et al., aves de los órdenes Falconiformes y Strigiformes de Europa y 1999), en diversos Galliformes del mundo (Yamaguti, 1961) y Norteamérica (Borgsteede et al., 2003; Sanmartín et al., 2004; en Anseriformes de Brasil (Vicente et al., 1995). Tabla 4). En la zona holártica, se ha identificado los capiláridos El hallazgo de Capillaria sp. s. l.en el intestino delgado de intestinales Baruscapillaria falconis (Goeze, 1782) Baruš & gallinas de Valdivia (Torres et al., 1974b), podría corresponder a Sergeeva, 1990 y Pterothominx caundinflata (Yamaguti, 1961; un ejemplar no identificado de alguna de las especies Baruš & Sergeeva, 1990a; Borgsteede et al., 2003); y algunas previamente registradas en gallinas de Chile (Tagle, 1966; no identificadas (Ferrer et al., 2004) (Tabla 4). En la mucosa Torres et al., 1974b); u otras presentes en Chile como C. esofágica de rapaces, se ha hallado Eucoleus dispar columbae, en otras aves y mencionadas entre los parásitos de las (Dujardin, 1845) López-Neyra, 1947, E. suppereri Kutzer, gallinas por la literatura (Ruff & Norton, 1997). Otras especies Frey & Kotremba, 1980 y E. contortus (Thominx contorta), de Capillariidae intestinales de la gallina, no registradas en consideradas sinónimas (Ferrer et al., 2004; Sanmartín et al., Chile, son A. bursata (Freitas & Almeida 1934), C. anatis 2004). También en este hábitat se ha encontrado Orni- (Schrank 1790), C. gallinae Cheng, 1982; C. uruguayensis thocapillaria cylindrica (Eberth, 1863) Baruš & Sergeeva, Calzada, 1937, B. montevidensis (Calzada, 1937) (Vicente et al., 1990 (López-Neyra, 1947; Baruš & Sergeeva, 1990b). (Tabla 1995; Ruff & Norton, 1997; Gibson, 2004). En el caso de las 4). palomas asilvestradas, se halló un 3% [Intensidad: 1-8 (17)] de Baruscapillaria obsignata (Madsen, 1945) Moravec, 1982 Capillaria sp. s. l. de Chillán (González-Acuña et al., 2004b), [sin. Capillaria obsignata Madsen, 1945] ha sido hallada en en que podría corresponder a algunas de las especies anteriormente el intestino delgado de gallinas provenientes de Valdivia mencionadas para palomas (Tabla 3b). (González et al., 1974; Torres et al., 1974b) y palomas Se han realizado hallazgos de Capillaria sp. s. l. en asilvestradas de Santiago (Toro et al., 1999). Mundialmente ha intestinos de gaviotas dominicanas (Larus dominicanus) del sido diagnosticada típicamente en en intestino delgados y ciegos estuario del río Valdivia (Torres et al., 1982), de los lagos

35 San Martín-Órdenes

Tabla 4 - Lista de Capillariidaepp recolectados en aves rapaces del mundo. Especie Hábitat Hospedadores Lugar Citas

Eucoleus dispar (Dujardin, Eo Buteo buteo, B. jamaicencis, Galicia Okulewicz (1988) 1845) B. lineatus, Accipiter nisus, Cataluña Kinsella et al. (1998) López-Neyra, 1947 A.gentilis, Falco peregrinus, Austria, Krone (2000) Sin. E. suppereri, E. contortus, F. tinnunculus, F. subbuteo, Alemania, Kinsella et al. (2001) Thominx contorta Circus aeruginosus, C. Rep. Checa Lierz et al. (2002) pygargus, Milvus milvus, Polonia Borgsteede et al. (2003) Circaetus gallicus, , Pernis Países Bajos Krone et al. (2003) apivorus, Haliaeetus albicilla, Francia Forrester & Spalding (2003) H. leucocephalus,Strix aluco, Alemania Ferrer et al. (2004) Strix varia USA Sanmartín et al. (2004) Finlandia Krone et al. (2006)

Baruscapillaria falconis ID Buteo borealis, B. buteo USA López-Neyra (1947) (Goeze, 1782) B. lagopus, B. lineatus, Canadá Read (1949) Baruš et Sergeeva, 1990a Accipiter, A. gentilis, A. Austria Ramalingam & Samuel (1978) Sin. Capillaria falconis (Goeze, trivirgatus,Circus, Asio Alemania Yamaguti (1961) 1782) López-Neyra, 1946 wilsonianus, Aegolius Países Bajos Hoberg et al. (1989) acadicus, Bubo v. virginianus, Taiwán Kinsella et al. (1996) Bubo bubo, F. tinnunculus,F. Rep. Checa Baruš &Sergeeva (1990a) sparverius, Aquila pomarina, España Illescas et al. (1993) Athene noctua, Asio otus, Kinsella et al. (2001) H. leucocephalus, Pandion Frantová (2002) haliaetus, Strix occidentalis, Borgsteede et al. (2003) Strix varia Forrester & Spalding (2003) Su & Fei (2004)

Capillaria tenuissima ID, tb Et B. buteo, A. nisus, A. gentilis, Alemania Kutzer et al. (1982) (Rudolphi, 1809) Yamaguti, F. tinnunculus, C. pygargus, Austria Okulewicz (1988) 1941 M. migrans, Haliaeetus Polonia Uchida et al. (1991) Sin. Thomix tenuissima albicilla, Milvago chimango, Rep. Checa Illescas et al. (1993) Tyto alba, Strix aluco, Strix Países Bajos Thebault (1988) uralensis, Strix varia, Athene Francia Krone (2000) noctua, Asio otus, Bubo España Kinsella et al. (2001) virginianus USA Frantová (2002) Japón Borgsteede et al. (2003) Chile Krone et al. (2003) Gibson (2004) Sanmartín et al. (2004) San Martín et al. (2006)

Capillaria strigis (Froelich, Strix, Asio, Syrnium, Nyctala, Europa López-Neyra (1947) 1802) Bubo, Carine, Galucidium, Japón Yamaguti (1961) López-Neyra, 1947 Archibuteo

Capillaria newzealandica Ninox novaehollandiae N. Zelandia Johnston & Mawson Yamaguti, 1961 (1944), Sin. Capillaria strigis Johnston Yamaguti (1961) et Mawson, 1944

36 Diversidad de Trichinelloidea en Chile

Tabla 4 - Lista de Capillariidaepp recolectados en aves rapaces del mundo (continuación). Especie Hábitat Hospedadores Lugar Citas

Pterothominx caudinfl ata I Falco tinnunculus Países Bajos Borgsteede et al. (2003) (Molin, 1858) Moravec, 1982 Registro Sin. Aonchotheca caudinfl ata, excepcional Capillaria caudinfl ata

Ornithocapillaria cylindrica Eo B. buteo, B. vulgaris, F. Europa López-Neyra (1947) (Eberth, 1863) Baruš et sparverius Cuba Yamaguti (1961) Sergeeva, 1990b Baruš & Sergeeva (1990b) Sin. Capillaria cylindrica (Eberth, 1863) Travassos, 1915

Capillaria sp. ID A. gentilis, A. nisus, B. buteo, Cataluña Ferrer et al. (2004) C. gallicus, C. cyaneus España

Capillaria sp. ID F. tinnunculus, A. nisus Países Bajos Borgsteede et al. (2003) Hembras dañadas B. buteo, Asio fl ammeus Strix aluco

Eo = esófago; Et = estómago; I = intestino; ID = intestino delgado.

Huillinco, en la Isla de Chiloé (Torres et al., 1991), Yelcho Valdivia (CONAMA Xª región de Los Lagos & UACh, 2004; (Torres et al.et al., 1992), Caburga y Llanquihue (Torres et al. Araya, 2005). Posiblemente, se trate de la especie C. droumondi 1993) (región de los Lagos). Además, hay hallazgos de parásitos Travassos, 1915, que ha sido descrita en el intestino de dicho del intestino de gaviota cáhuil (Larus maculipennis) de los lagos hospedador proveniente de Brasil (Vicente et al., 1995). Yelcho (Torres et al., 1992), Llanquihue y Puyehue (Torres et Recientemente, hay un registro de Capillaria (identificada al., 1993) (región de Los Lagos). Entre los registros de como Thominx sp.) en el Tyrannidae, fiofío Elaenia albiceps Capillaria sp. en Laridae, está el hallazgo en gaviota de pico chilensis. Hellmayr, 1927, en la provincia de Ñuble (Reyes, rojo (Larus novaehollandiae scopulinus) de Nueva Zelanda 2008). (Fredensborg et al., 2004). Baruscapillaria jaenshi (Johnston & Mawson, 1945) Moravec, 1982 fue identificada en L. Trichinellidae Ward, 1907. Existen registros de la especie novaehollandiae y otras especies del género Larus de Australia no encapsulada Trichinella pseudospiralis Garkavi, 1972, en (Yamaguti, 1961). Eucoleus contortus (sin. C. laricola aves carnívoras de las familias Falconidae, Accipitridae, Wassilkowa, 1930; Moravec, comunicación personal) es una Cathartidae (Lindsay et al., 1995; Kinne & Wernery, 2000), especie considerada común entre las especies de gaviotas a nivel Strigidae y Tytonidae (Strigiformes) (Pozio et al., 1999) y otros mundial (Threlfall, 1967; Yamaguti, 1961; Bosch et al. 2000) y casos de infecciones en córvidos e incluso gallinas domésticas, puede ser frecuente en aves marinas de Chile. También se halló pero hasta ahora sólo han sido obtenidas de las zonas Paleártica, Capillaria sp. en el sistema digestivo de Podiceps major Neártica y Oceanía (Pozio, 2005). (Boddaert) en el estuario del río Valdivia (Torres et al., 1982). No hay otros registros de Capillaria en esta especie, Trichuridae Railliet, 1915. Es considerada una familia de aunque en Podicipedidae se han registrado las especies C. parásitos de mamíferos, pero se han registrado huevos de pachyderma (Linstow, 1877) sp. inquirendum y B. podicipitis Trichuris en aves del Paraíso de Papua Nueva Guinea (Yamaguti, 1941) Moravec, 1982 en Podicepididae de Europa (Varghese, 1987). y Japón, respectivamente (Yamaguti, 1961). Además, los especimenes podrían corresponder a la misma especie no (3) Trichinelloidea hospedados por Reptilia Laurenti, 1768 identificada para gaviota dominicana en ese trabajo (Torres et y Amphibia Linnaeus, 1758. al., 1982). En esta revisión no se han encontrado trabajos que registren Se colectó Capillaria sp. de intestinos delgado y grueso de especies de Trichinelloidea en anfibios o reptiles, obtenidos cisne cuello negro (Cygnus melanocoryphus) en la Provincia de dentro del territorio nacional hasta el momento.

37 San Martín-Órdenes

Capillariidae Néveu-Lemaire, 1936. Se han realizado marina de Puerto Montt (Sepúlveda et al., 2004). Existe un varios trabajos sobre las especies de Capillariidae que infectan a registro de Capillaria sp. en el bagre de mar, Aphos porosus anfibios y reptiles (Moravec & Spratt, 1998; Moravec, 2001), (Valenciennes, 1837) (Batrachoididae, Batrachoidiformes), determinando los géneros que infectan a ambas clases (Tabla 1). capturado en el sector de San Juan, en la confluencia de los Con respecto a los anfibios chilenos, Puga (1994) y Garin & estuarios de los ríos Valdivia y Torneagalones (Región de Los González-Acuña (2008) realizaron recopilaciones de helmintos Ríos) (Torres et al., 1993). Se puede agregar, a este listado, el de anfibios de Chile, sin encontrar ningún Trichinelloidea, en hallazgo de Capillaria (Procapillaria) sp. dentro de los ciegos alguna de las 48 especies de anfibios nativas o la única pilóricos del granadero, Macrourus whitsoni (Macrouridae, introducida (Xenopus laevis Daudin) (Frost, 2004), que Gadiformes) proveniente del Mar de Weddell antártico (Walter corresponden exclusivamente a Anura. Mundialmente, eran et al., 2002; Rocka, 2002), parte del cual está dentro del cerca de 12 especies de Capillaria en anfibios y parecen ser territorio chileno antártico. Yamaguti (1961) recopiló 37 todas heteroxenas (Justine & Bain, 1987). Varias especies de especies de Capillaria en peces y son bastante más a la fecha. Capillaria habitan en el tracto intestinal de esta clase, e.g. Muchas de las especies del grupo pertenecen al género Capillaria petiti Justine & Bain, 1987 del sapo marino (Bufo Pseudocapillaria (Moravec et al., 2000a; Moravec, 2001). marinus) en Brasil y Capillaria sp. en la especie Atelopus Además, se registró Ornithocapillaria appendiculata (Freitas, bomolochus del Perú (Iannacone, 2003). Otras especies tienen 1933) en peces del Lago Pátzcuaro de México que las habrían hábitats más inusuales, como Pseudocapillaroides xenopi (sin. ingerido de las heces de aves marinas (Moravec et al., Capillaria xenopodis Wade, 1982) que afecta la epidermis de la 2000b). rana africana de uña (Moravec & Cosgrove, 1982; Wade, 1982), con una alta morbilidad y mortalidad de esta especie en Trichosomoididae Hall, 1916. Incluye unas 12 especies de cautiverio (Stephens et al., 1987). Huffmanella Moravec, 1987 que afectan la piel, mucosas de la En cuanto al grupo de los reptiles chilenos, se han realizado vejiga natatoria, de los arcos branquiales, serosas, musculatura e pocos estudios en general, más en su helmintofauna. De acuerdo incluso huesos de especies de Osteicthyes y Condricthyes en a la revisión de Garin & González-Acuña (2008), no se ha diversos lugares de la Tierra, cuyos ciclos no son conocidos realizado ningún registro de Capillaridae en alguna de las 94 completamente (Moravec, 2001; Justine, 2004; 2005). especies de reptiles recopiladas por Veloso et al. (1995) que incluye a las tortugas marinas, considerando que Yamaguti Cystoopsidae Skrjabin, 1923. Incluye al género monotípico (1961) recopiló 13 especies parásitas en el mundo. Cystoopsis Wagner, 1867 con dos especies de parásitos histozoicos, altamente especializadas (Moravec, 1999; 2001), C. Trichinellidae Ward, 1907. Algunas especies no acipenseri Wagner, 1987 que produce vesículas cutáneas en encapsuladas de Trichinella parasitan a reptiles (Kapel et al., esturiones, Acipenser spp. (Acipenseridae, Acipenseriformes, 1998; Pozio et al., 2004a). Trichinella zimbabwensis infecta al Osteichthyes) provenientes de zonas templadas holárticas y C. cocodrilo del Nilo (Crocodylus niloticus) de Zimbabwe (Pozio atractostei Moravec & Salgado-Maldonado, 2003 que fue et al., 2002) y T. papuae al cocodrilo de agua salada (C. encontrada en el tejido subcutáneo de Atractosteus tropicus Gill porosus), de Oceanía (Pozio et al., 2004b). (Lepisosteidae, Semionotiformes, Osteichthyes), en México (Moravec & Salgado-Maldonado, 2003). Dioctowittidae Chabaud & Le Van Hoa, 1960. Es una familia poco conocida que incluye al género Dioctowittus Trichinellidae Ward, 1907. No ha sido descrita como capaz Chabaud & Le Van Hoa, 1968 y ha sido registrada en la cavidad de infectar naturalmente a las clases vertebradas inferiores serosa de algunas especies de serpientes y varanos de la ecozona (anfibios y peces), de acuerdo a Pozio & La Rosa (2005). australiana (Jones, 1978; 1988). Moravec (1999) afirma que los peces sirven cómo hospedadores paraténicos para larvas de Trichinella. Pozio & La Rosa (2005) (4) Trichinelloidea hospedados por Pisces Linnaeus, 1758. alimentaron pirañas (Serrasalmus spp.) con músculos de ratones infectados con larvas de las especies que pueden desarrollar sus Capillariidae Néveu-Lemaire, 1936. Es la familia más rica ciclos completamente en animales poiquilotermos (T. papuae, T. en especies, incluyendo unas 54 especies y subspecies válidas zimbabwensis), sin desarrollar la infección. junto a 9 géneros parasitando el tracto digestivo e hígado de peces (Moravec, 1999). A la fecha hay sólo 5 registrosde (5) Trichinelloidea hospedados por invertebrados Capillariidae descritos, en las cerca de 1027 especies nativas y 19 introducidas de peces de Chile (Pequeño, 1989) y sólo en los Capillariidae Néveu-Lemaire, 1936. Incluye a algunos Actinopterygii (Osteichtyes). Se describió Capillaria sp. en el nemátodos que utilizan a oligoquetos como hospedadores estómago de un lenguado fino, Paralichthys adspersus paraténicos en ciclos homoxenos o intermedios, en ciclos (Steindaehner, 1867) (Paralichthyidae, Pleuronectiformes) en el heteroxenos. En Chile, no hay registros de Capillariidae en este norte, en una playa de la ciudad de Antofagasta (Oliva et al., grupo amplio, siendo inexistentes los trabajos sobre helmintos 1996). También, se obtuvo Capillaria sp. en la pejerrata de invertebrados. Sólo se conoce las características de los ciclos Nezumia pulchella (Pequeño, 1971) (Macrouridae, Gadiformes) de transmisión de unos 9 géneros de Capillariidae (Moravec et del Océano Pacífico, zona central (Salinas et al., 2008); en la al., 1987). Dentro de éstos, las especies de Capillariidae, que se corvina Cilus gilberti (Abbott, 1899) de Talcahuano (Garcías et conoce que incluyen invertebrados como hospedadores, y han al., 2001) y en el blanquillo (pez béntico) Prolatilus jugularis sido registradas en Chile son P. caudinflata, P. plica, E. (Valenciennes, 1833) (Sciaenidae, Perciformes) de la zona aerophilus y E. annulatus.

38 Diversidad de Trichinelloidea en Chile

Trichinellidae Ward, 1907. También ha sido descrita en El conocimiento de la familia Capillariidae es muy algunos artrópodos (Kapel, 2000). Larvas de mosca Sarcophaga incompleto (Moravec et al., 1987; Okulewicz & Zalesny, 2005), argyrostoma (Sarcophagidae) pueden mantener larvas de presentando una taxonomía muy controversial en cuanto al Trichinella capaces de infectar experimentalmente a ratones. De número de géneros (Zhu et al., 2000). Además, constituye un este modo, larvas de mosca como éstas, pueden actuar como grupo amplio y aparentemente muy homogéneo, pero que en hospedadores paraténicos para larvas de T. spiralis, y mantener realidad incluye especies sinoxenas (varias especies relacionadas al parásito en el medio, pero de manera limitada en comparación en un mismo hospedador) y polixenas (Morgan, 1932), a mamíferos carroñeros o caníbales (Maroli & Pozio, 2000). abarcando hábitats muy disímiles en el espectro total de hospedadores vertebrados (Okulewicz & Zalesny, 2005). Por su Discusión parte, Trichinellidae presenta una gran cantidad de trabajos, pero principalmente realizados en unas pocas especies domésticas o La biodiversidad parasitaria es tan rica que cualquier cálculo sinantrópicas. Hay evidencia de que otros vertebrados de Chile de ella resulta subestimado (Pérez-Ponce de León & García, podrían ser afectados por Trichinella, ya que se diagnosticó T. 2001), lo que se debe a que cualquier organismo que se estudie spiralis en Argentina, en el zorro chilla, P. griseus (Canidae), en puede albergar interna o externamente algún tipo de parásito el peludo patagónico, Chaetophractus villosus (Edentata) que (Esch & Fernández, 1993). De esta manera, al hablar de también son nativas de Chile y en el roedor Graomys diversidad biológica, la conservación de los parásitos ocuparía griseaflavus (Neghme & Schenone 1970; Pozio, 2000). En la un lugar preponderante, pero que presenta aspectos éticos y actualidad, varias son las especies identificadas en este género problemas únicos, como son los programas coordinados de monotípico, aunque no se han registrado otros trabajos que erradicación global, una imagen pública negativa, y un muestren la presencia de algunas de ellas en Sudamérica o equivocado consenso general de una diversidad de menor valía ecozona neotropical (Pozio, 2005). Además, todos los hallazgos que la de sus hospedadores (Daszak & Cunningham, 2002). han sido asumidos como de la especie tipo (T. spiralis s. l.), y no En este contexto, el registro de especies de parásitos de se han realizado estudios de PCR (Zarlenga et al., 2001a) para Chile, se enfoca principalmente como un problema sanitario, diagnosticar la especie precisa. Se han realizado muy pocos restringido a unas pocas especies (el hombre y principalmente estudios en especies atípicas o poco importantes en la animales de tipo productivo, domésticos, exóticos y sinan- transmisión, como es el caso de mamíferos y aves silvestres, los trópicos), siendo escasas las especies nativas de hospedadores, que no han presentado resultados positivos (Álvarez et al., 1970; lo que también se aprecia para el caso de Trichinelloidea (Tablas Cherres, 2004; San Martín et al., 2006), dificultando, además, el 3a- c). De ahí que la mayoría de las especies identificadas de hallazgo de especies no encapsuladas que se han encontrado en esta superfamilia, son cosmopolitas (como muchos de sus casos restringidos (Pozio, 2005). hospedadores), Mammalia y luego Aves, en su mayoría, Hasta la fecha, no ha habido registros de especies de las exóticas. Muchos de ellos son Capillaria (sensu lato) sp., familias Dioctowittidae, Cystoopsidae o Anatrichosomatidae, habiendo escasos hallazgos de especies consideradas nativas y cuya distribución es restringida en cuanto a información, ámbito que puedan ser endémicas (e.g. especies de Trichuris en de hospedadores y por aspectos evolutivos y ecológicos. De ahí roedores nativos). Esto se relaciona a la tendencia mundial, ya que cualquier hallazgo futuro pueda ser posible en animales que a diferencia de las especies de Capillariidae que parasitan exóticos. aves y mamíferos domésticos, el conocimiento de la biología y El aporte de los estudios parasitológicos a los programas de ecología de los helmintos de hospedadores silvestres, es investigación de la biodiversidad, es en cuanto al conocimiento fragmentario (Okulewicz & Zalesny, 2005). sobre la evolución de interacciones ecológicas y de estructura de La identificación de las especies de Trichinelloidea puede las comunidades y ecosistemas (incluido el ecosistema urbano) parecer innecesaria para fines veterinarios de rutina (Georgi et (Pérez-Ponce de León & García, 2001), lo que permite su al., 1990), pero puede ser valiosa para la determinación de utilización como pruebas contemporáneas de biodiversidad, ya aspectos epidemiológicos y de transmisión, como para en tiempo evolutivo(Gardner & Campbell, 1992). Esto, llevado determinar la fuente y su control, como es en el caso de especies al contexto transdisciplinario de la medicina de la conservación zoonóticas (Dunn et al., 2002), y además, para lograr un (Aguirre et al., 2002), reune aspectos epidemio-epizootiológicos, tratamiento eficaz de una parasitosis (Vásquez et al., 1997). infectológicos y patológicos, entre otros, que abarcan la salud Tradicionalmente, la identificación de especies de parásitos se humana, animal y ecosistémica. realiza a través de técnicas morfológicas o biométricas, pero La patogenicidad de los miembros de Trichinelloidea, para el caso de las especies de esta superfamilia el diagnóstico se especialmente Capillariidae, depende de la localización de los complica por la relativa poca diferenciación entre ellas y por la nemátodos y de la edad de los hospedadores y de la intensidad aparición de diferentes morfotipos como ocurre para Capilla- de la infección (Okulewicz & Zalesny, 2005). En mamíferos, los ridae (Zhu et al., 2000). De este modo, para la identificación de adultos de Eucoleus aerophilus habitan en los pulmones, los diferentes taxa de Trichinelloidea, se requiere incorporar el ocasionando una bronquitis y/o neumonía verminosa de grado uso de herramientas de análisis biotecnológicas, útiles para variable y con síntomas típicos (King et al., 1990), en algunos estudios de filogenia, caracterización y diferenciación de casos asociada a animales inmunodeprimidos e infecciones especies muy difíciles de diferenciar morfológicamente (Pozio et mixtas (e.g. gatos infectados con el virus de la al., 1999; Zhu et al., 2000; Pozio et al., 2002), y posterior inmunodeficiencia felina) (Barrs et al., 2000). Esta especie de desarrollo de pruebas para identificación de uso clínico y nemátodo requiere de la lombriz de tierra como hospedador paleoparasitológico (Oliveros et al., 1998; Zarlenga et al., 2001a intermedio (King et al., 1990). Además, E. aerophilus es y b; Martinez et al., 2003). potencialmente zoonótica, produciendo la capilariosis pulmonar

39 San Martín-Órdenes

en personas de diferentes partes del mundo (Acha & Szyfres, parásito y las aves ictiófagas los hospedadores definitivos 2003). Una especie patológicamente similar, pero no registrada naturales (Cross & Basaca-Sevilla, 1991; Moravec, 2001). Los en Chile, es Eucoleus boehmi, que habita en la mucosa de los parásitos provocan una enteritis leve con alteraciones senos paranasales y vías nasales de perros, ocasionando varios histopatológicas, que puede llevar una emaciación severa y casos de descarga nasal crónica y cambios conductuales para muerte de personas (Lu et al., 2006). tratar de expeler el parásito (Evinger et al., 1985; King et al., Trichinellidae es una de las familias de parásitos más 1990). estudiados por su importancia en salud pública. Las especies de Se han descrito varios casos de gatos y perros domésticos Trichinella producen la triquinosis o triquinelosis que se inicia infectados con Capillariidae, a nivel de la vejiga urinaria con el consumo de carne cruda o mal cocida (Acha & Szyfres, (Pearsonema plica, P. feliscati) (Wilson-Hanson & Prescott, 2003; Ribicich et al., 2004). Las consecuencias clínicas de las 1982; Bedard et al., 2002), con aparición de signos, como diferentes infecciones de especies de Trichinella van de hematuria (van Veen, 2002). inaparente a otras diversas, incluyendo conjuntivitis, edema Calodium hepaticum es una especie polixena importante periocular, fiebre, enteritis, miositis muy dolorosa y muerte porque ha sido registrada en más de 40 especies de mamíferos (Capó & Despommier, 1996), convirtiendo a la triquinelosis en hospedadores, de varios órdenes, además de ser zoonótica la zoonosis parasitaria más importante, de las transmitidas por (principalmente para niños de 1 a 5 años) (Davoust et al., 1997; alimento (Mitreva & Jasmer, 2006). Sawamura et al., 1999; Ruas et al., 2003). Este parásito se En cuanto a Trichuridae, hay varias especies que tienen desarrolla a través de un ciclo de vida atípico, que requiere para importancia en salud humana y animal. Trichuris trichiura es su continuidad la muerte del hospedador simultáneamente una especie que parasita al hombre y otros Primates en varias intermedio y final (Okulewicz et al., 2003). Su transmisión es partes del mundo. Además, se ha registrado el traspaso del favorecida por el canibalismo de las ratas (Farhang-Azad, 1977), parásito a Canidae, especialmente perros, zorros y lobos (Petavy en las cuales produce lesiones granulomatosas, necrosis y et al., 1990; Epe et al., 1993; Guberti et al., 1993), de modo que fibrosis hepáticas (capilariosis hepática) (Sawamura et al., 1999; tiene un potencial antropozoonótico. El helminto produce una de Ceruti et al., 2001; Ruas et al., 2003). En humanos presenta una las infecciones gastrointestinales más importantes (Pederson & tríada sintomatológica significativa con fiebre alta persistente, Murrel, 2001), asintomática en la mayoría de los casos, con hepatomegalia y eosinofilia excesiva (Pannenbecker et al., 1990, síntomas leves (desnutrición y anemia) a severos, como colitis Choe et al., 1993). ulcerativa y prolapso rectal (Bundy & Cooper, 1989; Ramdath et Dentro de los animales de producción es posible que se al., 1995; Williams-Blangero et al., 2002). En Chile, también la presente contaminación cruzada, con A. bovis (y también T. parasitosis ha sido asociada a la aparición de la apendicitis ovis) desde ganado doméstico tradicional a camélidos aguda, con una baja frecuencia (Martínez et al., 2006) y es domésticos, por los hallazgos de huevos de Capillaria sp. (y considerada, en algunos casos de infección masiva, de también Trichuris sp.) en alpacas y llamas (e.g. Valenzuela et pronóstico sombrío si no se realiza tratamiento (Sapunar et al., al., 1998), que podrían ser importantes para la ganadería de 1999). Es transmitida de hospedador a hospedador con un paso camélidos sudamericanos (Rojas, 1988). obligatorio por el suelo de los huevos a través de las heces Los efectos de Capillariidae en aves generalmente son (geohelminto) y embrionan en condiciones específicas de advertidos durante la necropsia, cuando se puede encontrar un temperatura, humedad y oxigenación adecuada (Martinez, gran número de parásitos en la ingluvia o en el intestino con 2003). Esto se relaciona a que su distribución sea mayor en las inflamación catarral que puede llevar a la emaciación o debilidad zona sur del país, debido a diferencias regionales notorias con de las aves (Kaufmann, 1996). Por ejemplo, Eucoleus contortus relación al tipo de suelo, humedad y además, costumbres ocasiona hiperemia de las mucosas y mucositis en primer lugar, (Bórquez et al., 2004). Se han descrito en el mundo algunos llevando a necrosis, alteración de las características del tracto casos de la presencia de T. vulpis en infecciones de personas, alimentario y otros síntomas, como retención de alimento, presentando signos de colitis mucosa, diarrea, tenesmo, caquexia y disnea, entre otros (Betlejewska et al., 2002). hematoquexia e incluso disentería (Vázquez et al., 1997; Aunque no hay estudios en Chile, la familia Capillariidae Vázquez & Valencia, 1998; Dunn et al., 2002) y en un caso tiene importancia en la ictiopatología de acuariofilia y mezclada con T. trichiura (Vázquez et al., 1997; Vázquez & producción de peces exóticos. De acuerdo a la literatura, los Valencia, 1998). Sin embargo, posiblemente sean muchos más Cichlidae (Perciformes) (e.g. disco, Symphysodon discus; pez los casos no reconocidos, porque clínicamente se observan como ángel o escalar, Pterophyllum scalare) y el siluro acorazado, una tricocefalosis común o bien como una tricocefalosis Callichthys callichtys (Callichthyidae, Siluriformes) parecen ser refractaria a tratamiento (Vázquez et al., 1997). Aunque el especialmentes susceptibles a estos parásitos (Butcher, 2000, tratamiento es el mismo, es conveniente la identificación de la Scott, 2000), los cuales les producen ulceraciones intestinales, especie, para asegurarse que la fuente canina sea tratada (Dunn heces mucosas, anorexia y emaciación (Butcher, 2000). et al., 2002). Un efecto indirecto de especies de Trichuris es el Paracapillaria (Crossicapillaria) philippinensis (Chitwood, que se ha comprobado de T. suis, que puede actuar de manera Velásquez & Salazar, 1968) Moravec, 2001 (sin. Capillaria o sinérgica en cerdos, para el desarrollo de Campylobacter jejuni Aonchotheca philippinensis) es el agente etiológico de la (Jones, Orcutt & Little, 1931) Veron & Chatelain, 1973, que es capilariosis intestinal de humanos (hospedador accidental) en una bacteria que causa la campilobacteriasis, una enfermedad países de Asia oriental, sur y occidental y ocasionalmente en el emergente importante en humanos, transmitida por cerdos Norte de África, medio Oriente y Europa (Cross & Basaca- (Mansfield et al., 2003). Sevilla, 1991; Moravec, 1999; Lu et al., 2006). Se sabe que los En otros países, se han descrito algunos casos en que peces son los únicos hospedadores intermediarios de este especies de Anatrichosomatidae han afectado accidentalmente al

40 Diversidad de Trichinelloidea en Chile

hombre (Morishita & Tani, 1960, Lu et al., 2006), además Andwanter, pone en evidencia el estrés al cual estas aves animales domésticos, como un gato de Sudáfrica (Lange et al., fueron sometidas por la contaminación antropogénica del 1980) y otro del Sudoeste de los Estados Unidos, el cual sufrió humedal (CONAMA Xª región de Los Lagos & UACh, una pododermatitis ulcerativa (Ramiro-Ibañez et al., 2002). 2004). Es por ello que al establecerse las llamadas zonas de También, está descrito un perro con una dermatitis supurativa amortiguamiento alrededor de reservas de la biosfera, se debe (Hendrix et al., 1987) y un hurón con nódulos cutáneos considerar el potencial impacto de las actividades antrópicas (Ramiro-Ibañez et al., 2002). (Daszak et al., 2001) y de los parásitos de animales De las asociaciones parásito-hospedador se puede obtener domésticos hacia la fauna silvestre y viceversa (Pérez-Ponce información sobre la ecología y etología de sus hospedadores, de León & García, 2001). sus poblaciones y ecosistemas (Pérez-Ponce de León & García, En conclusión, falta mucho por saber de la presencia e 2001, Daszak et al., 2001). Estos procesos son importantes en la identidad de la helmintofauna chilena, particularmente de los llamada interfaz de enfermedades de vida silvestre/ganado, que Trichinelloidea. Al parecer esta superfamilia tiene una distri- lleva a la interacción entre especies silvestres y domésticas y sus bución vasta y seguramente de una envergadura insos- parásitos y que surge como consecuencia de la fragmentación de pechada, conocida en unos cuantos focos de estudio y de unas hábitats y de la colonización humana (Kock, 2005). Esta interfaz cuantas especies. Las implicancias ecológicas y de actúa como un reservorio potencial y con efecto multiplicador conservación de los Trichinelloidea, sobre sus hospedadores para la infección (o infestación) de animales, llevando a la y el ecosistema, reflejan a las correspondientes a otros alteración de su conducta y en consecuencia, de los procesos múltiples grupos de parásitos. Es por ello que los parásitos evolutivos y ecológicos que regulan la biodiversidad. Esto lleva deben ser considerados en la conservación de la biodiversidad a la extinción de algunas especies (disminuiría la biodiversidad y total de Chile. riqueza de especies) y favorece a unas pocas generalistas dentro de las comunidades (Suzán et al., 2000). De esta manera, los Agradecimientos parásitos pueden utilizarse como organismos indicadores ecológicos para el monitoreo del estado (“salud”) de los Al Dr. Daniel González-Acuña (Facultad de Med. Vet., ecosistemas (Pérez-Ponce de León & García, 2001, Marcogliese, Universidad de Concepción, Chile) por su apoyo para la 2005). realización de este trabajo. Al Dr. Fred H. Borgsteede (Institute Particularmente, esta recopilación de Trichinelloidea expone for animal Science and Health, Países Bajos) y al Dr. František la posibilidad de transmisión desde animales domésticos a fauna Moravec (Institute of Parasitology, Academy of Sciences de nativa, como sucede con la especie polixena y generalista P. República Checa), por la información aportada amablemente caudinflata, posiblemente introducida con aves domésticas y para enriquecer este trabajo. encontrada en varias especies de aves silvestres como la endémica perdiz chilena (Hinojosa-Sáez & González-Acuña, 2005). El problema se complica con especies de hospedadores Referencias amenazados, a los cuales las infecciones podrían afectar su la viabilidad, e.g. el aguará-guazú (Chrysocyon brachyurus) Acha P. & Szyfres, B.2003. Zoonosis y Enfermedades infectado con Capillaria sp. (Pearsonema plica?) (Beldomenico Transmisibles Comunes al Hombre y a los Animales. et al., 2002) y el gato Geoffroy (Oncifelis geoffroyi) infectado Volumen III Parasitosis. 3ª ed. Washington, OPS. 403 pp. con Capillaria sp. y Trichuris campanula Linstow, 1889 Aguirre, J. 2006. Comparación de Dos Técnicas Copro- (Beldomenico et al., 2005), ambos en Argentina. En Chile, éste lógicas para el Diagnóstico de Endoparásitos del Perro. es el caso del huemul (Hippocamellus. bissulcus), especie Memoria de título, Méd. Vet. Universidad Austral de Chile, amenazada por sus poblaciones bajas y altamente fragmentadas Valdivia, Chile. (Deer Specialist Group, 1996), y que presenta infecciones con Trichuris sp. (Aldridge y Montecinos, 1998), posiblemente T. Aguirre A. A; Ostfeld, R. S.; Tabor, G. M.; House, C. & Pearl, ovis u otro proveniente de ganado doméstico. Se estima que las M. C. (Ed). 2002. Conservation Medicine: Ecological enfermedades transmitidas por el ganado están entre las Health in Practice. New York, Oxford University Press. amenazas principales para la especie (Povilitis, 1998). 407 pp. También, está el caso de las infecciones con Capillaria sp. y Alarcón, U. 2005. Estudio Taxonómico de la Fauna Para- Trichuris sp. de camélidos domésticos (Valenzuela t al., 1998). sitaria del Tracto Gastrointestinal de Zorro Gris Es posible que estos parásitos puedan afectar a una subespecie (Pseudalopex griseus, Gray 1837), en la XIIª Región de amenazada de guanaco (L. guanicoe huanacus) (South American MAGALLANES y Antártica Chilena. Memoria de título, Camelid Specialist Group, 1996a) y a la vicuña (Vicugna Med. Vet. Universidad Austral de Chile, Valdivia, Chile. vicugna), que si bien es cierto, actualmente se encuentra en bajo Alcaíno, H. & Arenas, X. 1981. Antecedentes sobre triquinosis riesgo, ésto se debe a programas enfocados a su conservación en Chile. Monografías de Medicina Veterinaria, 3: (2) [en (South American Camelid Specialist Group, 1996b). línea] http://www.monografiasveterinaria.uchile.cl/CDA/ El surgimiento de enfermedades transmisibles de especies mon_vet_articulo/0,1412,SCID%253D7278%2526ISID% silvestres puede estar relacionado a otros factores antropo- 253D401%2526PRT%253D0,00.html (Consulta: 31 de génicos y estrés ambiental (Daszak et al., 2001; Lafferty & agosto, 2007). Holt, 2003). El caso del hallazgo de Capillaria sp. s. l. (entre Alcaíno, H. & Gorman, T. 1999. Parásitos de los animales otros parásitos) del cisne de cuello negro, con una preva- domésticos en Chile. Parasitología al Día, 2: 33-41. lencia alta (93,5%) en el Santuario de la Naturaleza Carlos

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52 Lundiana 10(1):53-72, 2009 © 2011 Instituto de Ciências Biológicas - UFMG ISSN 1676-6180 Two new gall-inducing genera and species of Eriococcidae (Hemiptera) on Malvaceae and Anacardiaceae from the Neotropics

Chris Hodgson1, Thiago A. Magalhães2 & Douglass Miller3 1 Department of Biodiversity and Biological Systematics, The National Museum of Wales, Cathays Park, Cardiff, CF10 3NP, UK. Email: [email protected]. 2 Departamento de Botânica, Universidade Federal de Minas Gerais, Av. Antonio Carlos 6627, Belo Horizonte, Minas Geras, Brazil. 3 Systematic Entomology Laboratory, Beltsville Agricultural Research Center, U.S. Department of Agriculture, Beltsville, Maryland 20705, USA. Email: [email protected]

Abstract This paper describes two new genera and species of gall-inducing Eriococcidae from the Neotropics: Eriogallococcus isaias Hodgson & Magalhães gen. & sp. nov. from Brazil, which forms tall conical galls on the leaflets of Pseudobombax grandiflorum (Malvaceae), and Dromedaricoccus hansoni Hodgson & Miller gen. & sp. nov. from Costa Rica, in bulbous swellings on the young stems, petioles and underside of the mid-veins of leaflets of Astronium graveolens (Anacardiaceae). The adult female, adult male, pupa, 2nd- instar male and crawler of E. isaias are described and illustrated but only the adult female and adult male of D. hansoni are described and illustrated. Keys are provided for the identification of (i) all eriococcid genera now known from the Neotropics as recognised by Hodgson & Miller (2010) based on the morphology of the adult female and (ii) all Neotropical genera based on adult males for which this stage is known.

Keywords: Sternorrhyncha, Coccoidea, taxonomy, identification, immatures, host-plants.

Introduction (2002) and Cook & Gullan (2004) suggest that there are three major lineages in the Eriococcidae sensu lato. The fauna The family Eriococcidae or felt scales is the fourth largest currently known from the Neotropics falls into two of these family of scale insects (Hemiptera: Sternorrhyncha: Coccoidea) lineages, that which is basically Gondwanan in origin (Ben-Dov et al. 2010). It is most abundant in the Southern (encompassing Australia, New Zealand and South America) and hemisphere, particularly in New Zealand and Australia but is the more widespread acanthococcid clade (Cook & Gullan, almost certainly as abundant in South America which is less well 2004; Kondo et al., 2006). Clearly, therefore there are likely to studied. The status of the family in South America has been be major changes in the classification of this family in the near recently reviewed by Kozár (2009) and Hodgson & Miller future. (2010), although they used slightly different generic concepts. For a recent history of the study of this family in South Kozár (2009) concluded that 67 species of Eriococcidae in 27 America, see Hodgson & Miller (2010). What is striking about genera were known from the Neotropical Region whilst the eriococcid genera currently known from the Neotropics is Hodgson & Miller (2010) considered that there were 72 the high percentage of species that induce galls. The present recognisable species in 24 genera known from South America paper describes two further gall-inducing genera and species (i.e., minus Central America and the rest of the Caribbean). from the Neotropics, one from Costa Rica which induces However, Kozár’s placement of some of the species differed bulbous swellings on the twigs, petioles and main leaf veins of from that of Hodgson & Miller and further species have been Astronium graveolens (Anacardiaceae), and the other from described since Kozár’s paper was published. Brazil where it induces tall conical galls on the upper leaf There is mounting evidence that the family Eriococcidae is surface of Pseudobombax grandiflorum (Malvaceae). non-monophyletic – indeed, molecular analyses by Cook et al. Materials and methods

Received: 06-VI-10 Recently collected specimens were slide mounted in the Accepted: 15-I-10 usual way (see Henderson & Hodgson (2000)) except that all Distributed: 13-IX-11 specimens were left in cold KOH (about 20°C) for 3-4 days

53 Hodgson et al.

rather than being gently heated in warm KOH. Terminology collections of UFMG, Belo Horizonte, Brazil; USNM – The in the descriptions follows that of Hodgson & Miller (2010) National Museum of Natural History, Beltsville, Maryland, and Hodgson et al. (2004). Material examined is shown as USA, and BMNH- The Natural History Museum, London, (for example) 2/5 adff (= 2 slides with a total of 5 adult UK; BME – Bohart Museum of Entomology, University of females). Depository abbreviations are: Taxonomic California, Davis, USA.

Key to the Eriococcidae of the Neotropical Region based on the morphology of adult females

1. Legs present, sometimes greatly reduced or located near anal opening ...... 5 – Legs absent ...... 2

2(1) Conspicuously enlarged setae (excluding marginal setae) absent from dorsum ...... 3 – Conspicuously enlarged setae present on dorsum, either enlarged and narrow and restricted to posterior abdominal segments or cupolate-shaped and robust, scattered over thorax and abdomen ...... 4

3(2) Antennae segmented; quinquelocular pores restricted to mostly near thoracic spiracles, absent from dorsum ...... Pseudocapulinia – Antennae each represented by an unsegmented knob; quinquelocular pores present on both body surfaces ...... Carpochloroides

4(2) Enlarged setae of 2 types present, cupolate-shaped setae on anterior abdomen, thorax, and head, and elongate setae on posterior abdominal segments ...... Macracanthopyga – Only enlarged cupolate-shaped setae present, scattered over dorsum ...... Apiococcus

5(1) Antennae with 6 or more segments ...... 12 – Antennae with 5 or fewer segments...... 6

6(5) Dorsum of mature adult with a large sclerotised area over thorax or abdomen; without conical spinose setae on dorsum ...... 7 – Dorsum of mature adult without a large sclerotised area over thorax or abdomen; with conical spinose setae somewhere on dorsum ...... 8

7(6) Legs poorly developed; abdomen attenuated; mature adult female with large sclerotised hump on about metathorax ...... Dromedaricoccus – Legs fairly-well developed; abdomen not attenuated, body almost round; mature adult female with large area of sclerotisation on abdomen...... Eriogallococcus

8(6) Without ring of tubular ducts surrounding apex of abdomen ...... 9 – With ring of tubular ducts surrounding apex of abdomen ...... Capulinia

9(8) Legs large, well developed; dorsum of abdomen membranous ...... 10 – Legs small, abortive; dorsum of abdomen sclerotised ...... Aculeococcus

10(9) Enlarged setae not grouped in circular area on thorax and head ...... 11 – Enlarged setae grouped in circular area on thorax and head ...... Neotectococcus (in part)

11(10) Anal lobes protruding, heavily sclerotized ...... Pseudotectococcus – Anal lobes absent or very small, unsclerotized ...... Tectococcus (in part)

12(5) Anal lobes absent or, if present (sclerotised or not), not protruding noticeably past posterior apex of abdomen ...... 24 – Anal lobes present, clearly protruding from posterior apex of abdomen ...... 13

13(12) Macrotubular ducts present on dorsum ...... 17 – Macrotubular ducts absent from dorsum ...... 14

14(13) Antennae 6 segmented; without a cluster of spinose setae ventrally between meso- and prothoracic legs ...... 15 – Antennae 8 segmented; with a cluster of spinose setae ventrally between meso- and prothoracic legs ...... Eriobalachowskya

15(14) Loculate pores absent from spiracular atria; anal ring with 8 setae and with a double row of pores ...... 16 – Loculate pores present in spiracular atria; anal ring with 10 setae and with a single row of pores ...... Poliloculus

54 New genera and species of Eriococcidae

16(15) Dorsal setae large, conspicuously spiniform; translucent pores on hind coxa represented by large openings ...... Icelococcus – Dorsal setae small, slightly spiniform; translucent pores on hind coxa represented by small dots ...... Intecticoccus

17(13) At least some macrotubular ducts on dorsum with a conspicuous rim surrounding dermal orifice ...... 22 – Macrotubular ducts on dorsum without a conspicuous rim surrounding dermal orifice ...... 18

18(17) Without groups of microducts on dorsum of thorax and anterior abdominal segments ...... 19 – With conspicuous groups of microducts on dorsum of thorax and anterior abdominal segments ...... Hempelicoccus

19(18) Setae in medial areas of ventral abdomen with acute apices; translucent pores present on some, but not all, of the following hind leg segments: coxa, femur and tibia ...... 20 – Some setae in medial areas of ventral abdomen slightly capitate; translucent pores present on all of the following hind leg segments: coxa, femur and tibia ...... Coxicoccus

20(19) Anal lobes conspicuous and sclerotized...... 21 – Anal lobes small and unsclerotized ...... Oregmopyga (in part)

21(20) Anal lobes plate-like, not protruding strongly...... Chilecoccus (in part) – Anal lobes not plate-like, protruding strongly ...... Acanthococcus and Madarococcus

22(17) Venter with tubular ducts; dorsum without simple pores; cruciform pores absent ...... 23 – Venter without tubular ducts; dorsum with numerous simple pores; cruciform pores present on venter near body margin ...... Exallococcus

23(22) Venter with large clusters of tubular ducts; posterior abdomen without sclerotised nodules; anal lobes unsclerotised ...... Stibococcus (in part) – Venter with scattered tubular ducts; posterior abdomen with sclerotised nodules; anal lobes heavily sclerotised ...... Orafortis

24(12) Anal lobes without conspicuous sclerotisation...... 26 – Anal lobes conspicuously sclerotised ...... 25

25(24) Enlarged setae forming conspicuous band around body margin ...... Chilechiton – Enlarged setae not forming conspicuous band around body margin ...... Chilecoccus (in part)

26(24) Enlarged setae absent or, if present, not grouped in circular area on dorsum of thorax and head ...... 27 – Enlarged setae grouped in circular area on dorsum of thorax and head ...... Neotectococcus (in part)

27(26) Venter without large clusters of tubular ducts on abdomen ...... 28 – Venter with large clusters of tubular ducts on abdomen ...... Stibococcus (in part)

28(27) Largest dorsal macroducts without associated setae ...... 29 – Largest dorsal macroducts with 1–3 associated setae ...... Melzeria

29(28) Some dorsal setae cupolate; without winglike apodemes arising from mouthparts ...... 30 – Dorsal setae not cupolate; with large wing-like apodemes attached to mouthparts ...... Tectococcus (in part)

30(29) Anal lobes absent; anal ring non-cellular; ducts and pores sparse ...... Ovaticoccus – Anal lobes present; anal ring cellular; ducts and pores numerous...... Oregmopyga (in part)

Notes: based on the evidence provided by Cook & Gullan time but was considered unlikely to belong to the genus (2004), Hodgson & Miller (2010) transferred all species in the Opisthoscelis. Thus neither Eriococcus nor Opisthoscelis is Neotropics which were still assigned to Eriococcus Targioni included in the above key. Ovaticoccus Kloet is included in the Tozzetti to either Acanthococcus Signoret or to Hempelicoccus above key because of Ovaticoccus amplicoxae Williams & Kozár, and provided an appendix which listed the current Martin, from Belize. Ovaticoccus lahillei (Leonardi) was placement of all South America eriococcid species. However, it transferred to Eriococcus by González and then to was considered that many of these placements would change in Acanthococcus by Hodgson & Miller (2010). Recently, the the near future. In addition, Opisthoscelis prosopidis Kieffer & genus Madarococcus Hoy was revised by Hardy et al. (2008) Jorgensen was considered to be unrecognisable at the present based on nucleotide sequence data and morphology. As part of

55 Hodgson et al.

this revision, Hardy et al. transferred several species previously into the middle. The latter word is derived from the Latin galla, included in Eriococcus to Madarococcus. One effect of this f, which refers to a swelling or excrescence on a plant. The transfer was to make the generic diagnosis of Madarococcus name is treated as masculine. difficult due to the lack of diagnostic characters, which is why Madarococcus keys out with Acanthococcus above. Eriogallococcus isaias sp. nov. Hodgson & Magalhães

Eriogallococcus gen. nov. Hodgson & Magalhães Material studied. Holotype ad&: Brazil, State Park of Sumidouro, Lagoa Santa Municipality, Minas Gerais, on Type species: Eriogallococcus isaias sp. nov. Hodgson & Pseudobombax grandiflorum (Malvaceae), 23.ix.2009, Thiago Magalhães A. Magalhães (UFMG): 1/2 ad&&, holotype a young adult specimen before sclerotisation has set in; clearly labelled and Generic diagnosis: Adult female. Unmounted material. nearest to species name label. Inducing sharply conical galls on upper surfaces of leaves of Paratypes. Remaining specimen on holotype slide (UFMG) host plant but with gall orifice on the lower surface. Gall plus 25/10 ad&& (good to poor), 3 ?3rd-instar && nymphs (fair chamber quite elongate. Body of scale globose, almost round to to poor), 2 ?2nd-instar &&nymphs (good/poor), 11 1st-instar oval, perhaps broadest across metathorax. Youngest specimens nymphs (mainly fair to poor), 9 2nd-instar %% nymphs (mainly in alcohol pale pink but deep pink when mature. Mounted fair), pupa 3 (fair to poor) and 9 adult %% (fair to good) – all material. Body almost round to slightly egg-shaped. Anal with the same collection data as holotype but collected on lobes absent. Dorsum. Derm membranous on young various dates in 2009 (BMNH, USNM, UFMG). specimens, but developing a large circular sclerotised area on dorsum of abdomen on mature specimens. Dorsal setae rather Galls. Male and female galls similar in shape and size. few, most abundant posteriorly. Microtubular ducts with a Galls green and formed on dorsal surface of leaf. Actual gall distinctly sclerotised dermal rim, sparse across head, thorax and rather like a wizard’s hat, tall and narrow, pointed and, when anterior abdominal segments; absent more posteriorly. mature, generally bent, 8-12 mm long and 3-5 mm wide at base, Macrotubular ducts absent. Loculate pores, each mainly with 5 generally fattest about half-way along length. Gall orifice on loculi; frequent over most of dorsum but few or absent ventral leaf surface in middle of a strongly-developed rounded posteriorly. Anal lobes absent. Margin. Margin undefined, cone about 2-3 mm wide and 1-1.5 mm tall. Inner chamber without differentiated setae. Venter. Setae similar to those on quite broad, about 1.5-2 mm wide, with a narrow passage about dorsum, sparse. Microtubular ducts absent medially but present 2 mm long opening through the outer orifice. Walls of gall very sparsely along margin of head; structure similar to those on quite thick. dorsum. Macrotubular ducts and cruciform pores absent. Loculate pores extending onto venter between spiracles. Adult female (Fig. 1) Antennae appearing to be 3 segmented but setal distribution Described from 8 specimens in good to fair condition. suggesting perhaps 5 segmented. Clypeolabral shield with a pair of large broad, paddle-like apodemes extending antero-laterally; Unmounted material. As for generic diagnosis. Body 1.0- number of segments in labium uncertain, probably 2, with 3 3.0 mm long. pairs of setae. Eyespot distinct, laterad to antennae. Spiracles set in a cavity, entire spiracle surrounded by a sclerotised area in Mounted material. As for generic diagnosis. Body 1.0-2.0 oldest specimen. Legs short but moderately well-developed but mm long, 0.8-1.65 mm wide. Mature specimens with a large, tibia and tarsus often appearing fused; hind coxae not enlarged almost circular, area of sclerotisation on dorsal surface of and without translucent pores; each trochanter with 1 long and 1 abdomen. shorter seta on ventral surface; all tibia with 1 seta; tarsi slightly longer than tibiae, each with 2 setae; tarsal campaniform pore Dorsum. Derm of youngest specimens entirely mem- present; tarsal digitules capitate; claw digitules capitate, with branous but with a large circular sclerotised area developing one significantly broader than other; claws long and slender, on dorsum of abdomen in older specimens; sclerotised area each with a small denticle near apex. Anus possibly located on 0.83-1.5 mm long and 0.88-1.25 mm wide; intersegmental ventral surface, U-shaped, without pores or an anal ring. With a folds of some older specimens with a line of sclerotisations, pair of long setae posteriorly. Vulva placed between segments perhaps apodemes, between posterior abdominal segments. VII and VIII, surrounded by a group of flagellate setae. Dorsal setae rather few, most abundant posteriorly on abdomen and perhaps anteriorly on head but otherwise Comment. This new genus, Eriogallococcus, is immediately sparse; most setae fairly short and flagellate, 8-18 μm long separable from all other eriococcid genera known from the but a few longer posteriorly – up to 25-30 μm long. Neotropics in that the dorsum of the adult female has abundant Microtubular ducts, each with a distinctly sclerotised rim on loculate pores and develops a large area of sclerotisation on the derm, each about 10 μm long, with a central dark line down dorsum of the abdomen when mature. It is currently only outer duct; sparse across head, thorax and anterior abdominal known off Pseudobombax (Malvaceae) from Minas Gerais, segments becoming scarce or absent posteriorly. Brazil. Macrotubular ducts absent. Loculate pores, each convex and 6-8 μm wide and mainly with 5 loculi; frequent over most of Name derivation. Eriogallococcus is composed of the Latin dorsum, perhaps in sparse segmental rows, but absent name for the felt scales, namely Eriococcus, with “gall” inserted anteriorly on head and posteriorly on abdomen.

56 New genera and species of Eriococcidae

Figure 1 - Adult female of Eriogallococcus isaias Hodgson & Magalhães. Where B = dorsal microtubular duct; D = dorsal loculate pore; F = anal area; N = tibia + tarsus of metathoracic leg, P = antenna, and S = section through gall.

57 Hodgson et al.

Margin. Margin undefined; without differentiated marginal which had a non-sclerotised body (suggesting that it might have setae. Eyespot distinct, more or less round, 20-22 μm wide on recently moulted as most nymphs had a clearly sclerotised derm) margin laterad to antennae. had single loculate pores laterad to each spiracle and no macrotubular pores. As loculate pores are entirely absent in 1st- Venter. Setae mainly similar to those on dorsum but some instar nymphs, this specimen presumably represents a 2nd-instar longer, up to 65 or 70 μm long; mainly sparse, most abundant female. However, several other specimens (which had a anteriorly on head and posteriorly on abdomen; with 4 (or rarely sclerotised derm), also lacked macrotubular ducts (and therefore 5) pairs of longer setae in 2 longitudinal lines between antennae. could not be 2nd-instar males), but had more frequent loculate Microtubular ducts absent medially but present very sparsely pores, with some along the margin of the abdomen and a pair of along margin of head; structure similar to those on dorsum. pores dorsally on the prothorax. One of these specimens Macrotubular ducts and cruciform pores absent. Loculate pores, contained a pharate adult female. This instar, therefore, clearly similar to those on dorsum, present near margin, mainly between represents the pre-adult instar. Third-instar female nymphs are spiracles. presently unknown in the Eriococcidae. It is therefore Antennae appearing to be 3 segmented but setal distribution considered that further specimens should be studied before suggesting perhaps 5 segmented and therefore with apical 3 coming to any conclusion regarding the status of these segments more or less fused; length 85-105 μm; with 3 setae on specimens. scape, 1 on pedicel + campaniform pore; apex of each antenna with 2 very long “stiff” setae, each 38-45 μm. Clypeolabral Second-instar male (Fig. 2) shield with a pair of large broad, paddle-like apodemes extending antero-laterally; actual shield 125-155 μm long; Described from 5 specimens in fair to poor condition. length of shield + apodemes 180-310 μm; labium probably 2 segmented, with 3 pairs of setae. Spiracles: width of peritremes: Unmounted material. Body egg-shaped, broadest across 25-27 μm, set in a cavity 35-40 μm wide; entire spiracle anterior abdomen; segmentation rather distinct, particularly on surrounded by a sclerotised area in oldest specimen. Legs short abdomen. Specimens in alcohol slightly pink to deep red. but moderately well-developed but with tibia and tarsus often appearing fused; length of metathoracic leg (μm): coxa 70-90, Mounted material. Length 0.6-0.9, width 0.34-0.5 mm. trochanter + femur 90-105; tibia + tarsus 85-100, claw 16-20; Anal lobes absent. hind coxae not enlarged, without translucent pores, but with 3 setae; each trochanter with 1 long and 1 shorter seta on ventral Dorsum. Derm sclerotised in oldest specimens but maybe surface; femur with 2 setae; tibia with 1 seta; tarsi each with 3 membranous when young; with numerous dermal nodulations, setae; tarsal digitules capitate, subequal to length of claw particularly on head and posterior part of abdomen. Dorsal setae digitules; claw digitules capitate, each claw with one digitule rather few, possibly segmentally arranged; setae fairly short and significantly broader than other; each claw long and slender, flagellate, each about 10 μm long. Microtubular ducts absent. with a small denticle near apex. Anus possibly located on Macrotubular ducts present sparsely throughout, apparently ventral surface, U-shaped, without an anal ring, width about segmentally arranged; each with a broad, sclerotised outer 28-35 μm; with, just anteriorly, a pair of longer setae, 25-30 orifice, about 4.5 μm wide, a long outer ductule (8 μm long) μm long, plus a small group of 3 or 4 setae laterally on each with a cup-shaped inner end and an equally long inner side, each 20-50 μm long; also with one pair of very long ductule with a small terminal gland. Loculate pores, each setae laterad to anus, each about 130-180 μm. Vulva placed convex, 6 μm wide with 5 loculi, frequent marginally and between segments VII and VIII, surrounded by a group of submarginally on abdomen but scarce marginally on thorax flagellate setae. and absent on head.

Comment. Mature adult females of E. isaias are Margin. Margin perhaps defined by a line of short curved immediately separable from those of all other South setae near margin of dorsal sclerotisation, each about 8 μm long. American eriococcids due to the presence of the large area of Eyespot distinct, more or less round, 15-17 μm long on margin sclerotisation covering the dorsum. However, even young laterad to antennae. specimens are easily identified by the combination of: (i) moderately well-developed legs and antennae; (ii) dorsum Venter. Derm lightly sclerotised but without nodulations. with frequent loculate pores throughout; (iii) absence of Derm with small dermal spinules present almost throughout. macrotubular ducts and cruciform pores, and (iv) the reduced Setae few, mainly similar to those on dorsum, most 13-15 μm structure of the anus. The adult female of Dromedaricoccus long but longer near anus and mesad to meso- and metacoxae, hansoni Hodgson & Miller, described as new below, also has where up to 35 μm long; mainly sparse, most abundant a heavily sclerotised area on the dorsum, but can be posteriorly on abdomen; also 3 pairs of longer setae in 2 immediately separated by its elongate shape and absence of longitudinal lines between antennae, each up to 40 μm long. dorsal loculate pores. Microtubular ducts absent. Macrotubular ducts, similar to those on dorsum, present sparsely throughout. Cruciform pores absent. Second/third-instar females (not illustrated) Loculate pores mostly similar to those on dorsum but those nearest spiracles perhaps smaller (5 μm wide); present Several nymphal specimens were available that were clearly submarginally on posterior abdominal segments and near each neither 1st-instar nor 2nd-instar male nymphs. One specimen, spiracular peritreme.

58 New genera and species of Eriococcidae

Figure 2 - Second-instar male of Eriogallococcus isaias Hodgson & Magalhães. Where A = dorsal seta + dermal nodulations; C = dorsal macrotubular duct; D = dorsal loculate pore; E = eyespot with dermal nodulations; J = ventral macrotubular duct; K = ventral loculate pore; N = tibia + tarsus of metathoracic leg, and P = antenna.

59 Hodgson et al.

Antennae appearing to be 3 segmented but setal distribution marginal setae, each curved posteriorly and about 5 μm long. suggesting 5 segments, with apical three segments fused; length Eyespot more or less round, 12-14 μm wide on margin laterad to 63-66 μm; with 3 setae on scape, 1 on pedicel + campaniform antennae. pore; apex of each antenna with 2 long “stiff” setae, each 28-35 μm. Clypeolabral shield with small antero-lateral apodemes; Venter. Derm sclerotised but less so than dorsum and length of shield 100-125 μm; labium 2 segmented, with 3 pairs without nodulations except perhaps along margins. Derm of setae. Spiracles: width of peritremes: 10-12 μm, apodeme with small dermal spinules present at least posteriorly. Setae long, 20-30 μm long. Legs short but moderately well- few and setose, most about 10 μm long but with a few longer, developed; length of metathoracic leg (μm): coxa 55-57, those anterior to anus and mesad to metacoxae about 15 μm trochanter + femur 65-73; tibia 35-43, tarsus (subequal in length long, those mesad to mesocoxae longer, about 30 μm and to tibia) 36-43; claw 17; hind coxae not enlarged and without 3 pairs of interantennal setae up to 30 μm long. Micro- translucent pores but probably with 3 setae; each trochanter with and macrotubular ducts and loculate and cruciform pores 1 long and 1 shorter seta on ventral surface; femur with 2 setae; absent. tibia with 0 or 1 seta; tarsi with 2 or 3 setae; tarsal campaniform Antennae appearing to be 3 segmented but setal distribution pore present; tarsal digitules both capitate, offset, so that one suggesting perhaps 5 segmented, with apical 3 segments semi- much longer than other, apices subequal in length to those of fused; length 45-52 μm; with 3 setae on scape, 1 on pedicel + claw digitules; claw fairly long and slender, each with one campaniform pore; apex of each antenna with 2 long “stiff” digitule significantly broader than other; each claw with a small setae, each 35-50 μm long. Clypeolabral shield without antero- denticle. Anus possibly located on ventral surface, with a U- lateral apodemes; length of shield 105-125 μm; labium shaped sclerotisation, width about 16-18 μm, width of outer apparently 2 segmented, with 3 pairs of setae. Spiracles: width sclerotisation 21-23 μm; with 2 pairs of short setae just anterior of peritremes: 10-12 μm, apodeme possibly absent. Legs short to anus plus with a line of 4 setae more anteriorly to anus, most but moderately well-developed; length of metathoracic leg (μm): 20-35 μm long; plus further setae posteriorly; long posterior seta coxa 30-35, trochanter + femur 43-50; tibia 19-20, tarsus about 100-120 μm. (clearly much longer than tibia) 26-29; claw 13-14; coxa probably with 3 setae; each trochanter with possibly only 1 long Comment. The 2nd-instar male of E. isaias differ from all seta on ventral surface; tibia with 0 or 1 seta; tarsi each with 2 other instars in having macrotubular ducts and no microtubular setae; tarsal campaniform pore present; tarsal digitules offset, ducts; 2nd/3rd-instar and adult females have only microtubular one much longer than other and extending past claw digitules, ducts. longer digitule capitate, other flagellate; claw fairly long and slender, each with one digitule significantly broader than First-instar nymph (sex not determined) (Fig. 3) other; each claw with a small denticle. Anus possibly located on ventral surface, U-shaped, without an anal ring, width Described from 4 specimens in fair to poor condition, 3 about 5 μm; setae around anus probably distributed as on rather young and one much larger and pharate. adult female; each anal lobe with one long seta about 55 μm long. Unmounted material. Body oval; segmentation rather distinct, particularly on abdomen. Specimens in alcohol deep red. Comment. First-instar Eriogallococcus isaias are unusual for 1st-instar nymphs of scale insects in having the derm of both Mounted material. Length 0.32-0.62, width 0.17-0.40 mm. surfaces somewhat sclerotised. Other significant characters are: Anal lobes short but distinct on youngest specimens but (i) antennae reduced; (ii) dermal nodulations present throughout disappearing as body swells so that no lobes are apparent on dorsum; (iii) presence of two long “stiff” setae on apex of each oldest specimen. antenna; (iv) presence of microtubular ducts on dorsum (but absent from venter); (v) presence of a pair of short anal lobes on Dorsum. Derm distinctly sclerotised even on young youngest specimens; (vi) anus reduced to a small U-shaped specimens; young specimens with numerous dermal nodulations structure; (vii) tarsal digitules on all legs very different, with one throughout, nodulations largest and most distinct posteriorly and very long and capitate, other much shorter and setose, and (viii) along margins; old specimen much swollen and nodulations claw digitules dissimilar. absent although still indicated by darker oval areas on derm. In the key to 1st-instar nymphs of South American Dorsal setae rather few, apparently segmentally arranged, each eriococcids in Hodgson & Miller (2010), the nymphs of E. short with a blunt apex and about 4-5 μm long. Microtubular isaias key out (more or less!) to couplet 2 and to Tectococcus ducts, each about 7 μm long, present although distribution Hempel. However, the nymphs of these two genera are easily uncertain, but with 2 pairs on abdominal segment 1 and on separable as follows (character-states on T. ovatus Hempel in meso- and metathorax, perhaps only 1 pair on prothorax and 2 brackets): (i) all dorsal and marginal setae setose (marginal pairs on head. Macrotubular ducts and loculate pores absent. and medial lines of dorsal setae all cupolate); (ii) loculate Anal lobes present on either side of anus of youngest specimen, pores absent (loculate pores present on venter associated with each about 15 μm long, each with a long anal lobe seta, 60-65 spiracles); (iii) microtubular ducts absent from venter μm long. (present along ventral margins); (iv) claw digitules dissimilar (similar, both narrow); (v) tarsal digitules not both capitate Margin. Margin indicated by a major reduction in the size (both capitate), and (vi) apex of antennae each with 2 very of the dermal nodulations and the presence of a sparse line of long “stiff” setae (setae all much shorter).

60 New genera and species of Eriococcidae

Figure 3 - First-instar nymph of Eriogallococcus isaias Hodgson & Magalhães. Where A = dorsal seta; B = dorsal microtubular duct; F = anal area; L = marginal seta; N = tibia + tarsus of metathoracic leg, and P = antenna.

61 Hodgson et al.

Pupa (Fig. 4) total body length; body fairly setose, fleshy setae (fs) (Described from 3 specimens, 1 in fair condition, 2 poor, difficult to separate from hair-like setae (hs) but generally broken in half.) longer and less finely pointed (fs 15-27 μm long; hs 10-15 μm long) - due to similarity, most setae not differentiated in Unmounted material: pupa (and adult male) covered in a text below; length of fs on antennae shorter than width of rather sparse felt test, penial sheath extending posteriorly out of antennal segments. Wings about 0.65 total body length and felt coat. Material in alcohol colourless to pale pink. about 0.4 as wide as long.

Mounted material: body rather elongate, 1.38 mm long. Head: rather pointed anteriorly in dorsal view, but clearly Derm membranous apart from lightly sclerotised penial sheath. bulbous ventrally; length 155-180 μm; width across genae about Head fairly clearly demarcated but division between thorax and 200-223 μm. Median crest (mc) poorly demarcated, not abdomen unclear. Penial sheath unusually long and blunt. reticulated but slightly ridged; postoccipital ridge (por) distinct, with quite strong posterior ridges and weaker anterior ridges; Head: about 235-270 μm widest; without eyes or with many dorsal head setae (dhs), perhaps mainly fs; pores mouthparts. Antennae obscurely 5 segmented, each about 290- absent. Mid-cranial ridge absent; ventrally derm with 320 μm long. With 3 pairs of small setae on ventral surface longitudinal microridges and with 2-4 ventral mid-cranial ridge between antennae and 5 pairs dorsally plus 1 or 2 pairs laterally. setae (vmcrs) on each side. Genae (g) not reticulated but each with 1-4 hs genal setae (gs). Simple eyes (se): two pairs, each Thorax: legs short, anterior pair not reaching anterior round and subequal in size, 40-50 μm wide. Ocelli (o) quite margin of head; metathoracic legs each about 360-460 μm long; large, very convex and placed laterally, each 14-16 μm wide, without setae. Mesothoracic wing buds well developed, each situated just dorsad to where interocular ridge (ior) extends about 400 μm long and 135-155 μm wide; metathoracic wing anteriorly. Ocular sclerite (ocs) sclerotised and dorsally lightly buds absent. Spiracles small, width of anterior peritremes 18-21 reticulated between ocelli and dorsal simple eyes. Preocular μm wide; without spiracular loculate pores. Setae sparse on ridge (procr) short dorsally but with an interocular ridge (ior) both surfaces. extending posteriorly and fusing with postocular ridge (pocr) ventral to each ocellus. Postocular ridge (pocr) strongly Abdomen: caudal extensions on segment VII absent, those developed, extending dorsally past posterior margin of each on segment VIII rounded, with a single longer seta about 25-28 dorsal eye, almost reaching postoccipital ridge (por) medially. μm long, plus a short seta 8-15 μm long. Each abdominal Dorsal ocular setae absent. Ventral head setae (vhs) numerous, segment with a sparse band of about 4 short abdominal setae perhaps mainly fs, present both between ventral simple eye (vse) both dorsally and ventrally; also with 1 or 2 short dorsal pleural and around anterior and lateral margins of each vse. Tentorial setae and 1 short ventral pleural seta on each side. bridge absent. Cranial apophysis (ca) finger-like and blunt, Segment IX fused to penial sheath, cylindrical and lightly about 45 μm long. sclerotised, with anus on dorsal surface. Penial sheath together Antennae: 5-segmented and filiform; each 320-385 μm long with abdominal segment IX forming a nearly parallel-sided (ratio of total body length to antennal length 1:0.21). Scape cylinder extending from posterior end of abdomen; total length (scp): 35-39 μm long and 40-46 μm wide, with 2 or 3 hs about 190-200 μm and width 115-130 μm at base and 70-75 μm ventrally and 1 hs dorsally. Pedicel (pdc): length 33-46 μm, wide at apex. Penial sheath with 1 or 2 pairs of small setae on apex, width 33-40 μm, with distinct annular reticulations; with about 4 each about 8-16 μm long, plus a sclerotised triangular structure fs, 8 hs + (probably) 1 campaniform pore; fs about 11-24 μm about 30-35 μm long and 35-38 μm wide at base, slightly long. Segment III 133-155 μm long, broadest distally (about 15 constricted apically, where possibly bifid, apex about 8 μm wide. μm wide basally and up to 30 μm wide distally), with a short finger-like extension on apex; with about 23 setae + (possibly) 1 Comment. The homologies of the parts of the “penial antennal bristle (ab) but latter very similar to fs; segment IV sheath” are uncertain. The anterior part appears to relate to similar in shape to III but much shorter, about 48-85 μm long, abdominal segment IX; the triangular structure might be the with about 18 fs, 1 hs and perhaps an antennal bristle (ab) (very penial sheath proper – which leaves the intermediate part (more similar to fs); apical segment (V) rounded apically, about 95-108 than half its length) uncertain. However, although the penial μm long, with about 16 fs, 3 large and distinct ab + perhaps 2 or sheath of male eriococcids appears always to be composed of 3 smaller ab (similar to fs), 7-11 capitate setae (caps) + 1 sensilla abdominal segment IX fused with the actual penial sheath, the basiconica. structure of this penial sheath appears to be unique for an eriococcid pupa. In all other known eriococcid pupae, the Thorax. Prothorax: pronotal ridge (prnr) well developed penial sheath is more or less pointed quite unlike the rather and not fused dorsally; with a broad, slightly striated, cylindrical structure in E. isaias. triangular, lateral pronotal sclerite (prn); without lateral pronotal setae. With 1 pair of medial pronotal setae (mps). Adult male (Fig. 5) Post-tergital setae absent. Post-tergites not detected.

(Described from 6 specimens, all fair to poor, several Sternum (stn1) not sclerotised but with slight, almost circular, missing antennae). striations; with a strong transverse ridge; median ridge short

or absent; with 3-5 fs prosternal setae (stn1s) + 1 or 2

Mounted material: of moderate size, total body length anteprosternal setae (astn1s). Antemesospiracular setae 1.5-1.8 mm; antennae short, 5-segmented, only about 1/4th absent.

62 New genera and species of Eriococcidae

Figure 4 - Pupa of Eriogallococcus isaias Hodgson & Magalhães. Where an = anus, ads = dorsal abdominal setae; avs = ventral abdominal setae;

dps = dorsal pleural setae; ps = penial sheath; sp2, sp3 = anterior and posterior spiracles; vps = ventral pleural setae, and II, VIII and IX = abdominal segments II, VIII and IX.

63 Hodgson et al.

Figure 5 - Adult male of Eriogallococcus isaias Hodgson & Magalhães. Where A = cranial apophysis, C = hair-like seta; D = fleshy seta; E = apex of penial sheath; F = distal end of metathoracis leg; X =dermal reticulations on dorsal surface of head; Y = dermal microridges on ventral surface of head. And where aas = ante-anal setae; ab = antennal bristle; ads = dorsal abdominal setae; aed = aedeagus; amss = anterior

metasternal setae; an = anus; astn1s = anteprosternal setae; avs = ventral abdominal setae; bra = basal rod; c = claw; caps = capitate setae; cdt = claw digitule; ceVIII = caudal extension to abdominal segment VIII; cx = coxa; dhs = dorsal head setae; dps = dorsal pleural setae; dse = dorsal simple eye; dss = dorsospiracular setae; epm3 =metepimeron; eps2 = mesepisternum; f = furca; fm = femora; fs = fleshy seta; gp = glandular pouch; gps = glandular pouch setae; gs = genal setae; hs = hair-like setae; ior = interocular ridge; lpl = lateroleurite; mc = median crest; mps = medial pronotal setae; mr = marginal ridge; mts = metatergal setae; o = ocellus; ocs = ocular sclerite; pa =

postalare; pcr2 = mesoprecoxal ridge; pdc = pedicel; plr3 = metapleural ridge; pm2s = postmesospiracular setae; pm3s = postmetaspiracular setae; pmss = posterior metasternal setae; pn2 = mesopostnotum; pna = postnotal apophysis; pnp = postnotal wing process; pocr = postocular ridge; por = preoral ridge; prar = prealare ridge; prn = pronotal sclerite; prnr = pronotal ridge; procr = preocular ridge; prsc = prescutum; prscs = prescutal setae; ps = penial sheath; pscr = prescutal ridge; psp = penial sheath sensilla; pss = penial sheath setae; ser = subepisternal ridge; scl = scutellum; sclr = scutellar ridge; scls = scutellar setae; scp = scape; sct = scutum; scts = scutal setae; sp2 =

anterior spiracle; sp3 = posterior spiracle; stn1s = prosternal setae; stn2 = basisternum; ta = tarsus; tcp = tarsal campaniform pore; tdt = tarsal digitule; ti = tibia; tr = trochanter; teg = tegular; vhs = ventral head setae; vmcrs = ventral midcranial ridge setae; vps = ventral pleural setae, and vse = ventral simple eye And where II, VI, VII, VIII and IX = abdominal segments II, VI, VII, VIII and IX.

64 New genera and species of Eriococcidae

Mesothorax: prescutum (prsc) transversely oval, 95-125 μm differentiated, each 30 μm long; tarsal campaniform pore (tcp) long and 150-180 μm wide; sclerotised but not reticulated; with present; tarsal digitules (tdt) distinctly longer than claws, 5-7 prescutal setae (prscs); prescutal ridges (pscr) and prescutal without apical knobs. Claws (c) quite long and rather straight, suture (pscs) well developed. Scutum (sct): median area subequal to width of tarsi, with a distinct small denticle; length: sclerotised but not reticulated, distance between prescutum and III: 21-25 μm; claw digitules (cdt) longer than claw, dissimilar, scutellum about 33-55 μm; scutal setae (scts) 0 or 1 pair; lateral one clearly broader than other, both with apical knobs. margins sclerotised but not reticulated; prealare ridge (prar) weak. Scutellum (scl) 135-165 μm wide and 58-75 μm long; Abdomen: segments I-VII: tergites (at) and sternites with an inverted U-shaped scutellar ridge (sclr); probably not unsclerotised; without obvious oval membranous areas in inter- tubular and lacking a foramen; scutellar setae (scls): 0 or 1 pair segmental membranes. Caudal extension of segment VII absent. hs; posterior notal wing process (pnp) quite long and sclerotised. Dorsal setae (ads) (totals, mainly fs): segments I & II 2-4; III-

Basisternum (stn2) 210-305 μm wide and 130-145 μm long; VII 8-16, each about 25-27 μm long. Pleural setae: dorsopleural median ridge absent, but bounded anteriorly by a moderately setae (dps): 1-3, mainly hs; ventropleural setae (vps) (on each strong marginal ridge (mr) and posteriorly by strong precoxal side, mainly fs): III-VI 1; VII 0-5. Ventral setae (avs) (totals, ridges (pcr2); with many basisternal setae (stn2s); lateropleurite mainly fs): II-VII 15-25, each up to 45 μm long. Segment VIII: (lpl) narrow, poorly defined and without an extension from with a lightly sclerotised tergite (at) but no sternite; with 8-12 marginal ridge along anterior margin; furca (f) well developed, ante-anal setae dorsally, mainly fs; sternite with 10-15 ventral narrow-waisted, arms very divergent and extending almost to abdominal setae (avs) on each side; caudal extension (ce) anterior marginal ridge (much shorter on 1 specimen). rounded, with 1 long hs pleural seta (length 35-40 μm) + 1 short

Mesopostnotum (pn2) well developed; postnotal apophysis (pna) seta (about 40 μm long). Glandular pouches (gp) present, rather well developed and opening quite large. Area bounded deep; each without loculate pores around outer margin of pouch; anteriorly by scutellum and laterally and posteriorly by glandular pouch setae (gts) each about 80-100 μm long. mesopostnotum not sclerotised. Mesepisternum (eps2) not reticulated; subepisternal ridge (ser) well developed. Postalare Genital segment: total length of penial sheath (ps) 500-555 (pa) well developed; without postalare setae. Mesothoracic μm long (ratio of total body length to length of penial sheath + spiracle (sp2): width of peritreme 22-27 μm. Postmesospiracular segment IX 1:0.33); divided into two parts: anterior section setae (pm2s) abundant in an elongate group extending across (segment IX?) sclerotised, broad (width at base 105-125 μm, segment between spiracles; perhaps mainly fs. Tegula (teg) approximate length 95-100 μm); anal opening posteriorly on present, rarely with 1 tegular setae. dorsal surface; some specimens with a single long seta dorsally, about 35-40 μm long. Posterior part (penial sheath proper?) Metathorax: with 1 or 2 pairs hs metatergal setae (mts). very long, 450-460 μm long and 50-55 μm wide at base, almost Dorsospiracular setae (dss): about 4 on each side. parallel sided with a pointed apex; sclerotised; with 4 or 5 long Metapostnotum absent or small, poorly sclerotised. Dorsal part setae, each 40-60 μm long, near apex. Aedeagus (aed) long, of metapleural ridge absent, ventral part (plr3) well developed; almost as long as posterior part of penial sheath; length 400-460 episternum unsclerotised, with 5-10 postmetaspiracular setae μm, and narrow, 8-10 μm wide throughout most of length.

(eps3s) on each side; precoxal ridge (pcr3) absent. Metepimeron Basal rod (bra) short, perhaps 25-28 μm long. Penial sheath

(epm3) quite long, without setae. Antemetaspiracular setae with a few small sensilla (pss) near apex. absent. Metathoracic spiracle (sp3): width of peritreme about 23-25 μm. Metasternum membranous, with 3-10 anterior Comment: the adult male of E. isaias is immediately metasternal setae (amss) and 20-30 posterior metasternal setae separable from the males of other eriococcid genera known from (pmss). the Neotropics in having: (i) only 5-segmented antennae; (ii) an extremely long, fine penial sheath, and (iii) 0 or 1 tegular setae. Wings: hyaline, about 1.0-1.4 mm long and 425-475 μm Other significant characters are: (i) only one tarsal segment wide (ratio of length to width 1:0.38; ratio of total body length (otherwise only known in Dromedaricoccus hansoni Hodgson & to wing length 1:0.73); alar lobe, alar sensilla and alar setae Miller, described as new below); (ii) fleshy and hair-like setae absent. Hamulohalteres absent. very similar (otherwise known in Capulinia sallei Signoret); (iii) a denticle on the claw (otherwise known on Tectococcus ovatus Legs: metathoracic leg marginally longest. Coxae (cx): I: Hempel and D. hansoni.); (iv) capitate setae restricted to apical 95-112; II: 82-100; III: 103-115 μm long; coxa III with about antennae segment only (as on C. sallei and D. hansoni); (v) no 10-15 fs + 3-6 hs. Trochanter (tr) + femur (fm): I: 185-210; II: dermal pores (as on Pseudotectococcus anonae Hempel, C. 203-220; III: 220-245 μm long; trochanter III with 0-6 fs + 2 hs; sallei and D. hansoni); (vi) tibial spurs not differentiated from long trochanter seta about 55-60 μm long; femur III with about other spur-like setae on tibia (as on D. hansoni), and (vii) 23-30 fs + 2 or 3 hs. Tibia (ti): I: 130-165; II: 140-180; III: 145- antennal setae shorter than width of segment (also on D. 185 μm; tibia III with a total of about 25-30 setae, mainly hs, a hansoni). From the above comparisons, E. isaias would appear few becoming spur-like on distal third of leg, plus 1 or 2 fs on to be most similar to D. hansoni but the latter has a very short dorsal surface distally; apical spurs (tibs) not differentiated but penial sheath, 6-segmented antennae, extremely short and setose setae in this position 28-30 μm long. Tarsi (ta) 1 segmented: 60- tarsal digitules, and several tegular setae. 88; II: 75-90; III: 86-108 μm long (ratio of length of tibia III to length of tarsus III 1:0.6); tarsus III with 18-25 setae, mainly General Biology. Pseudobombax grandiflorum is a spur-like, but some on dorsal surface fs; tarsal spurs barely deciduous plant and is totally free of leaves from March to

65 Hodgson et al.

August. In the Gruta da Lapinha region in the State Park of male insects emerge from the galls to copulate with the females Sumidouro, Minas Gerais State, Brazil, the galls start which are sessile and stay inside the gall. The first-instar developing shortly after bud-burst in August and September nymphs or crawlers hatch inside the galls, exit through the when they become heavily infested with the galls of E. isaias, ostiole and disperse in November and December, but the site which are induced in the lower surface of the young leaflets. where they hibernate has not been determined. A new gall cycle Their development is concomitant with leaf sprouting until coincides with bud-burst the following year. maturation. The galls grow in about 30-40 days, are light green, glabrous, intralaminar, with an aciculate projection to the upper Etymology. This species name isaias is in honour of surface, and an open ostiole to the lower surface. No sexual Professor Rosy M.S. Isaias, Departamento de Botânica, dimorphism could be found in gall structure, and just one Universidade Federal de Minas Gerais, who has now discovered inducer occurs in each chamber. E. isaias is univoltine, and the two new species of gall-inducing Eriococcidae from Minas Gerais.

Key to instars of Eriogallococcus isaias

1. Wings or wing-buds present...... 2 – Wings or wing-buds absent ...... 3

2. Fully-developed wings present; head with 2 pairs of simple eyes ...... adult male – Wings only represented by wing buds; head without simple eyes ...... pupa & prepupa

3. Macrotubular ducts present; microtubular ducts absent ...... 2nd-instar male – Macrotubular ducts absent; microtubular ducts present ...... 4

4. Loculate pores frequent over entire dorsum, with more than 30 pores ...... adult female – Loculate pores absent or with fewer than 30 pores ...... 5

5. Loculate pores entirely absent ...... 1st-instar nymph – Loculate pores present at least near each spiracular peritreme ...... 2nd-/3rd-instar female

Dromedaricoccus gen. nov. Hodgson & Miller. apex. Spiracles each with a large U-shaped area of sclerotisation around peritreme on margin side. Legs all short and distorted, but Type species: Dromedaricoccus hansoni sp. nov. Hodgson apparently with all segments; claw rather variable in size, & Miller sometimes with a small denticle; claw digitules capitate and longer than claw. Vulva not detected. Generic diagnosis. Adult female (Fig. 6). An eriococcid inducing spherical galls on young stems, petioles and particularly Generic name derivation: Dromedaricoccus is composed of leaflets of host plant. Mounted material. Adult female with head dromedarius (m), Latin for one-humped camels, here referring and thorax round and swollen, narrowing abruptly to a long narrow to the sclerotised hump or boss on the dorsal surface, and abdomen, posterior segments of which concertina into more anterior Coccus, a word frequently used to describe scale insects. The segments. Derm mainly membranous but with a heavily sclerotised name is treated as masculine. boss or hump mediodorsally approximately on metathorax. Dorsum. Setae all rather small, often curved; frequent throughout Dromedaricoccus hansoni nov. sp. Hodgson & Miller on head and thorax (including dorsal boss) but scarce on narrow abdomen. Macro- and microtubular ducts absent. Loculate pores Material examined. Holotype &: Costa Rica, in galls on absent. With a group of sclerotised pores just anterior to anal ring. Astronium graveolens (Anacardiaceae) -.xi.1999, J. Lobo & Paul Anal lobes absent. Anus present just anterior to posterior apex of Hanson (USNM): 1/3 ad&& (holotype ad& left specimen on abdomen, without anal ring setae or pores. Margin. Not slide along with 2 adult paratype && in fair to good condition demarcated. Venter. Derm membranous apart from near spiracles (USNM)). Also: Paratype && with same collection data: and around mouthparts. Setae as on dorsum. Macrotubular ducts 6/9 ad&& (in fair to good condition but most somewhat twisted) absent. Microtubular ducts present anteriorly on head and laterally + 8 ad%% (in fair to good condition) (BMNH, BME, USNM). on at least prothorax. Loculate pores each with mainly 5 loculi; most abundant in a broad line between anterior and posterior coxae, Adult female (Fig. 6) and extending a long way laterally; a few possibly present on head between procoxae and antennae. Antennae probably 6 segmented, Unmounted material. Unknown. segmentation weakly demarcated, all segments ring-like. Frontal lobes absent. Clypeolabral shield quite small but embedded in a Mounted material. Total length 3.0–4.5 mm, length of strongly sclerotised area of unusual shape; labial segmentation narrow abdomen 1.5–2.5 mm; greatest width 1.5–2.0 mm. Head unclear, perhaps 2 segmented, possibly with only 2 pairs of setae on and thorax round and swollen as in generic diagnosis. Derm

66 New genera and species of Eriococcidae

Figure 6 - Adult female of Dromedaricoccus hansoni Hodgson & Miller. Where F = anus; G = seta; H = ventral microtubular duct; K = ventral

loculate pore; M = posterior spiracle; N = metathoracic leg; P = antenna; Q = pores near anus; R1, R2 = setae near anus; T = one side of mouthparts; X = side view of adult female, showing “hump”.

67 Hodgson et al.

mainly membranous but with a heavily sclerotised boss or hump the mesothorax. In addition, (i) the abdomen is drawn out into a mediodorsally approximately on metathorax, flattish on some narrow tube; (ii) the legs and antennae are much reduced; (iii) (younger?) specimens and highly convex on others, basal width there are no anal lobes; (iv) the anal ring is a sclerotised area, about 790–990 μm, greatest height about 670 μm and width of perhaps with 2 small setae laterally; and (v) each spiracle has a dorsal “plateau” about 445–480 μm. C-shaped area of sclerotisation laterally around the spiracular opening. No other eriococcid genus has this combination of Dorsum. Derm mostly membranous, segmentation obscure features in the adult female. apart from on narrow abdominal region. A heavily sclerotised boss present medially, probably on metathorax, as described Adult male (Fig. 7) above. Dorsal setae small, often curved, each 9–10 μm long; frequent throughout on head and thorax (including dorsal boss) Described from 8 specimens in mainly good condition. For but scarce on narrow abdomen; setae immediately around anus abbreviations, see Fig. 5. rather larger, mainly 23–28 μm long but some up to 35 μm along posterior margin of abdomen. Macro- and microtubular ducts Mounted material: total body length about 0.95–1.05 mm; absent. Dorsal pores restricted to a group of 5–8 oval, antennae short, about 1/4th total body length; body setose, sclerotised pores just anterior to anal ring, each 11–16 μm long particularly on head and venter; fleshy setae (fs) each about 16– and about 7 μm wide; other pores absent. Anal lobes absent. 18 μm long, often curved, not always easy to separate from fine Anus present just anterior to posterior apex of abdomen, without hair-like setae (hs); hs mainly about 8–10 μm long but some as anal ring setae or pores; appearing rather similar to anal ring of long as fs; short, stout fs absent. Loculate pores entirely absent. Cryptococcus; oval, about 40–42 μm long and 30–37 μm wide, Wings without either alar setae or sensilla. Hamulohalteres appearing to have a transverse slit with a small seta on either absent. Tarsi 1 segmented; tarsal digitules setose. Glandular side; presence of other setae perhaps variable but possibly with a pouches and glandular pouch setae present. small pair at posterior end. Head: approximately oval to almost round in dorsal view; Margin. Margin not demarcated and without marginal setae. width across genae about 200–205 μm; length of head about Eyespots apparently absent. 165–175 μm. Median crest (mc) represented by a faint ridge extending anteriorly from post-occipital ridge (por); not Venter. Derm membranous apart from sclerotised areas near reticulated; por distinct, extending laterally and slightly spiracles and around mouthparts. Setae as on dorsum; with 1 posteriorly; anterolateral arms absent; dorsal head setae (dhs) pair of interantennal setae, each about 21–30 μm long. abundant, mainly fs, but dhs absent between dorsal simple eyes Macrotubular ducts absent but microtubular ducts present (dse) and postocular ridge (pocr); head without pores. Mid- anteriorly on head and laterally on at least prothorax; each small, cranial ridge absent both dorsally and ventrally. Gena not about 6.5 μm long and about 1 μm wide, with a dark inner end; reticulated, with 15 or 16 fs + 2–7 hs genal setae (gs). Eyes: apparently without a dark, longitudinal inner line. Loculate with 2 pairs of round, simple eyes, subequal in size, each about pores each about 6.5 μm wide, with mainly 5 loculi (range 3– 30 μm wide. Ocelli (o) each 16–18 μm wide, not touching about 10) and a heavily sclerotised margin; most abundant in a postocular ridge (pocr). Ocular sclerite (ocs) barely sclerotised; broad band between anterior and posterior coxae, and extending reticulations barely visible, only obvious immediately around a long way laterally; a few possibly present on head between each simple eye. Preocular ridge (procr) extremely short, procoxae and antennae. represented only by an articulatory sclerite laterad to each scape; Antennae probably 6 segmented, segmentation weakly but also with a faint line extending posteriorly over dorsal demarkated, all segments ring-like, length 50–60 μm; scape simple eye (dse) to por (possibly an interocular ridge). perhaps quite wide; apex with at least 4 fleshy setae + some Postocular ridge (pocr) strongly developed, extending dorsally setose setae. Clypeolabral shield quite small, about 100–110 μm to about level with dorsal margin of each dse. Ventrally with long, but apparently embedded in a strongly sclerotised area of abundant ventral head setae (vhs), mainly fs, extending unusual shape (see Fig. 7T), 250–285 long and 200–235 wide at anteriorly to head apex and also around and between ventral anterior end; labial segmentation unclear, perhaps 2 segmented, simple eyes (vse) posteriorly. Preoral ridge distinct. Cranial possibly with only 2 pairs of setae on apex. Spiracles each with apophysis (ca) distinct, pointed, about 33 μm long. Mouth (mth) a large U-shaped area of sclerotisation around peritreme on apparently present rather far posteriorly (almost between margin side, each about 50 μm wide; inner peritreme 20–22 μm anterior coxae), with a pair of small lateral pores, perhaps wide; muscle plate + peritreme each about 65–70 μm long. Legs tentorial pits. all short and distorted, but apparently with all segments; claw Antennae: 6 segmented and filiform (occasionally apical 3 rather variable in size, from 10–22 μm long, sometimes with a or 4 segments variously fused), segment III longest; length small denticle; tarsal digitules capitate but generally shorter than about 250 μm long (ratio of total body length to antennal length claw; claw digitules capitate and longer than claw; translucent 1:0.25). Scape (scp): 28–32 μm long and 35–38 μm wide, with 3 pores absent. Vulva not detected on any specimen. hs setae on anterior and dorsal surface. Pedicel (pdc): length 37– 45 μm, width 34–37 μm; with faint concentric microridges Comment. Dromedaricoccus is a monotypic genus only throughout; with 14–19 fs, 5 hs setae + 1 campaniform known from Costa Rica. The adult female of D. hansoni can be sensillum. Flagellar segments 24–28 μm widest, but segment III immediately recognised by the general shape of the body and the very narrow basally; fs short, 13–18 μm long; lengths of circular, dome-shaped sclerotisation medially on the dorsum of segments (μm): III 74–86; IV 20–24; V 20–24; VI 50;

68 New genera and species of Eriococcidae

Figure 7 - Adult male of Dromedaricoccus hansoni Hodgson & Miller. Where A = cranial apophysis; B = side view of aedeagus; C = hair-like seta;

D = fleshy seta; F = distal end of metathoracic leg; mth = mouth; pcr3 = metaprecoxal ridge; pepcv = proepisternum + cervical sclerite ; pra = prealare ridge; tegs = tegular setae, and tp = triangular plate.

69 Hodgson et al.

approximate number of setae per segment: III 20–25 fs + 1 or 2 (tr) + femur (fm) I 125–145; II 140; III 140–145; metatrochanter hs; IV & V 10–15 fs + 0–2 hs, and VI 7 or 8 fs, 4 large and 1 with 8–12 setae, mainly fs; campaniform sensilla narrow, in a small antennal bristles (ab) + 7 or 8 capitate setae (caps); sensilla diagonal line; long trochanter seta differentiated, 43–60 μm basiconica not detected. long, placed much nearer proximal end of segment than normal; metafemur with about 6–8 fs + 5–7 hs. Tibia (ti) I 82–87; II 78– Thorax. Prothorax: pronotal ridge (prnr) present, not 83; III 82–87; metatibia with a total of about 10 setae, mainly apparently fused medially on dorsum; pronotal sclerite (prn) hs, a few becoming spur-like on distal third of leg; without distinct, each with faint ridging; without lateral pronotal, medial fleshy setae on dorsal surface; with 1 poorly defined tibial spur, pronotal and post-tergital setae. Post-tergite (pt) lightly 23–25 μm long. Tarsus (tar) I 66–83; II 53–62; III 60–65 (ratio sclerotised. Prosternum (stn1) with a distinct transverse ridge but of length of tibia III to that of tarsus III 1:0.73); tar 1 segmented; median ridge only hinted at with faint ridges; possibly without metatarsi with 10–13 setae, mainly spur-like but a few fs; tarsal apophyses laterally; with many fs + a few hs prosternal setae spurs poorly differentiated, length 20–22 μm; tarsal

(stn1s), extending anteriorly to area of ante-prosternal setae campaniform sensilla (cp) present; tarsal digitules (tdt) short and

(astn1s). Proepisternum + cervical sclerite (pepcv) showing setose. Claw short, subequal to width of tarsi, with a distinct nothing distinctive. Antemesospiracular setae absent. small denticle; length III: 15–18 μm; claw digitules (cdt) Mesothorax: prescutum (prsc) oval, 78–95 μm long, 128– distinctly longer than claw, with minute apical knobs, 1 perhaps 145 μm wide; sclerotised but not nodulated; with 4–6 prescutal slightly larger than other. setae (prscs) on each side; prescutal ridges (pscr) well developed; prescutal sclerites (pscs) only lightly sclerotised; Abdomen: segments I–VII: abdominal tergites (at) and prealare (pra) and triangular plates (tp) well developed. Scutum sternites (as) membranous; without obvious oval membranous (sct): median area sclerotised, without nodulations; distance areas in inter-segmental membranes. Pleurites unsclerotised. between prescutum and scutellum about 50–55 μm, with 1 or 2 Caudal extentions (ce) of segment VII absent. Abdominal dorsal scutal setae (scts) laterally on each side; setae absent medially; setae (ads) few, segments I–VII each with 1–4 fs + 0–4 hs. prealar ridge weak. Scutellum (scl) about 120 μm wide and 50 Pleural setae: each segment with about 6 fs + 2 hs dorsopleural μm long; with an inverted U-shaped scutellar ridge; probably not setae (dps) on each side, and usually with 2 fs + 1 hs tubular and lacking a foramen; scutellar setae (scls) 1 pair; ventropleural setae (vps) on each side. Abdominal ventral setae postnotal wing process (pnp) quite long, more or less transverse (avs) (on each side): II: abundant, mainly fs; III & IV many, and heavily sclerotised. Basisternum (stn2) 185–190 μm wide mainly fs; V–VII few, both fs and hs. and 120–125 μm long; median ridge absent; bounded anteriorly Segment VIII: at and as unsclerotised; tergite with 2 hs by a moderately strong marginal ridge (mr) and posteriorly by ante-anal setae (aas); sternite with 0–2 setae; caudal extention strong mesoprecoxal ridges (pcr2); with many fs basisternal setae (ce) small and rounded; with about 3 pleural setae, mainly fs but

(stn2s), mainly distributed nearer margins; lateropleurite (lpl) usually 1 much longer, up to 60 μm long. Glandular pouch (gp) narrow, with a short ridge anteriorly; furca (f) well developed, present, placed perhaps slightly more medially than usual, with a narrow-waisted, arms divergent and extending about 2/3rds to fairly narrow and deep pouch, each with pores restricted to anterior marginal ridge. Mesopostnotum (pn2) well developed; within pouch; each with 2 glandular pouch setae (gls) about 60– mesopostnotal apophysis (pna) well developed, with round 90 μm long. opening. Area bounded anteriorly by scutellum and laterally and Genital segment: penial sheath (ps) quite short, but broad posteriorly by mesopostnotum not sclerotised. Mesepisternum anteriorly (segment IX?), rapidly narrowing to a sharp apex;

(eps2) not reticulated; subepisternal ridge (ser) strongly total length 60–90 μm, greatest width 60–67 μm (ratio of total sclerotised. Postalare (pa) well developed; without postalare body length to length of penial sheath 1:0.08); anal opening setae. Anterior spiracle (sp2) small, width of peritreme about 18 medially on dorsal surface, 35–42 μm wide; with no setae on

μm. Postmesospiracular setae (pm2s) abundant, mainly fs, dorsal surface, but with a line of about 8 setae anterior to extending full width of segment. Tegular (teg) present, with 3 or aedeagus (aed), each 25–32 μm long, plus 2 pairs of penial 4 tegular setae (tegs) on each side. sheath setae (pss) near apex, each 21–25 μm long. Aedeagus Metathorax: metatergal setae (mts): 1 or 2 fs + 1–3 hs on each (aed) tapering slightly, and extending to tip of penial sheath; side. Dorsospiracular setae (dss): 9–11 fs + 0 or 1 hs on each side. length 58–70 μm, greatest width about 10 μm. Basal rod (bra)

Dorsal part of metapleural ridge (plr3) absent; ventral part short; present anterior to aedeagus; short. Penial sheath apparently metepisternum (eps3) unsclerotised, with 0–2 fs + 0–1 hs with a few small sensilla (psp) marginally near apex. postmetaspiracular setae (pm3s) on each side; metaprecoxal ridges

(pcr3) extremely short. Metepimeron (epm3) sclerotised but without Comment. The adult male of D. hansoni can be separated from setae. Antemetaspiracular setae absent. Posterior spiracle (sp3) of the other known Neotropical eriococcid males in having the moderate size: width of peritreme about 18 μm. Metasternum (stn3) following combination of characters: (i) 6 segmented antennae, with membranous and without metasternal apophyses; with a total of 5– fleshy setae much shorter than width of antennal segments; (ii) 14 fs + 0 hs anterior metasternal setae (amss) and many posterior capitate setae on the antennae restricted to apical segment; (iii) metasternal setae (pmss), mainly fs. antennal bristles apparently restricted to apical segment (or similar Wings: hyaline, 750–800 μm long, 350–375 μm wide (ratio to fleshy setae on previous 2 segments); (iv) penial sheath short, of total body length to wing length 1:0.78); alar lobe, alar only slightly longer than basal width; (v) fleshy setae not easily sensoria and alar setae absent. Hamulohalteres absent. separable from hair-like setae; (v) legs relatively small; (vi) tarsal Legs: subequal in length. Lengths (μm): coxa (cx) I 78–82; digitules unusually short; and (vii) head with many fleshy setae. II 75; III 78–82; metacoxae with 6 or 7 fs + 3–5 hs. Trochanter The males of most gall-inducing eriococcids have elongate

70 New genera and species of Eriococcidae

abdomens or long penial sheaths so as to facilitate reaching the female inside the gall. The male of D. hansoni appears to have no such adaptations unless the reduced size of the legs is in some way related to access to within the gall. However, perhaps copulation is here facilitated by the elongation of the abdomen of the adult female rather than that of the adult male?

General biology. Little is known about the general biology of D. hanseni. The galls are found on the young stems, petioles and mid-veins of the leaflets of the host plant, producing spherical swellings mainly on the underside of the leaflets. Old galls are very hard and difficult to cut with a knife. Although Paul Hansen reared several other insects from these galls, he believes that the eriococcid is the main gall-inducer. The other insects are probably mainly parasitoids and predators of D. hanseni: Eulophidae (Tetrastichinae), Eupelmidae, Eurytomidae and a few Cecidomyiidae. The latter he considered to be an inquiline and he also reared Platygasteridae from the gall which he considered was probably a parasitoid of the cecidomyid.

Etymology. This species is named in honour of Paul Hanson, who has collected several interesting gall-inducing scale insects in Costa Rica.

Key to the Genera of the Eriococcidae of the Neotropical Region based the morphology of the adult males

1 Antennae with 8 or fewer segments...... 5 – Antennae with 10 segments ...... 2

2(1) Penial sheath less than half length of abdomen ...... 3 – Penial sheath more than half length of abdomen ...... Capulinia

3(2) Antennae with long, narrow fleshy setae, similar to hair-like setae ...... 4 – Antennae with thicker fleshy setae, obviously different from hair-like setae ...... Acanthococcus

4(3) Glandular pouch shallow, with pores spreading out of pouch onto dorsum; glandular pouch setae short, only extending to about half length of penial sheath; dorsal abdominal setae not as abundant as ventral abdominal setae ...... Stibococcus – Glandular pouch deep, with pores restricted to within pouch; glandular pouch setae long, extending to about level with tip of penial sheath; dorsal abdominal setae more abundant than ventral abdominal setae ...... Carpochloroides

5(1) Glandular pouches absent; antennae 7 segmented; abdomen attenuated ...... Tectococcus – Glandular pouches present; antennae not 7 segmented; abdomen not attenuated ...... 6

6(5) Penial sheath very long, several times longer than basal width; antennae 5 segmented; genae each with few setae ...... Eriogallococcus – Penial sheath shorter, at most 3 times longer than basal width; antennae 6 or 8 segmented; genae each with many setae...... 7

7(6) Fleshy setae clearly differentiated from hair-like setae, each short and blunt; antennae 8 segmented; tarsi each 2 segmented ...... Pseudotectococcus – Fleshy setae very similar in structure to hair-like setae, each long with a sharp apex; antennae 6 segmented; tarsi each 1 segmented ...... Dromedaricaoccus

Discussion are known to induce galls in their host plants (Hodgson & Miller, 2010) (although the habit of several other species is not Of the 27 genera of Eriococcidae now known from the known). Of these, three induce galls on Myrtaceae, two on Neotropics, these two new genera can be easily distinguished Annonaceae and one on Fabaceae (the host families of the from the others by the presence of an area of moderate to heavy remainder are unknown, including that of Ovaticoccus sclerotisation on the dorsum on the mature adult females. amplicoxae, which was not included in Hodgson & Miller’s Eriogallococcus isaias is the first record of an eriococcid review as it is only known from Belize). collected on Malvaceae in the Neotropical Region while As pointed out in the Introduction, recent molecular Dromedaricoccus hanseni is only the second record on analyses have strongly suggested that the family Eriococcidae is Anacardiaceae (the other is Icelococcus lithreae Miller & non-monophyletic and consists of three separate clades (Cook et González from Chile). By far the most common host plant al., 2002; Cook & Gullan, 2004). Looking at the morphological family in this region is Myrtaceae (26%), followed by similarities between Eriogallococcus and Dromedaricoccus and Nothofagaceae (16%) and Fabaceae (14%). Of the 76 the genera studied in the above papers, it seems clear that these eriococcid species now known from the Neotropics, 12 (16%) two new genera fall within the Gondwanan clade.

71 Hodgson et al.

Acknowledgments Hardy, N.B., Gullan, P.J., Henderson, R.C. & Cook, L.G. 2008. Relationships among felt scales (Hemiptera: Chris Hodgson thanks the Department of Biodiversity and Coccoidea: Eriococcidae) of southern beech, Nothofagus Biological Systematics, The National Museum of Wales, (Nothofagaceae), with first descriptions of Australian Cardiff, for the use of their facilities and for their general species on the Nothofagus-feeding genus Madarococcus encouragement. Thiago Magalhães thanks the Plant Biology Hoy. Invertebrate Systematics, 22: 365-405. Post-Graduation Program and CAPES for financial support. We Henderson, R.C. & Hodgson, C.J. 2000. Coccidae (Insecta: also thank Ferenc Kozár, Gary Miller, and Alex Konstantinov Hemiptera: Coccoidea). Fauna of New Zealand, 41. 264 for helpful suggestions. pp. Hodgson, C.J. & Miller D.R. 2010. A review of the Eriococcid genera (Hemiptera: Sternorrhyncha: Coccoidea) of South References America. Zootaxa, 2459: 1-101. Ben-Dov, Y., Miller, D.R. & Gibson, G.A.P. 2009. ScaleNet – Hodgson, C.J., Gonçalves, S.J.M.R., Miller, D.R., & Isaias, Classification. http://www.sel.barc.usda.gov/scalenet/ R.M.S. 2004. A key to genera of Eriococcidae (Hemiptera: classif.htm Coccoidea) from the Neotropical region and a revision of Cook, L.G. & Gullan, P.J. 2004. The gall-inducing habit has Pseudotectococcus Hempel (Eriococcidae), a gall-inducing evolved multiple times among the eriococcid scale insects scale insect genus from Brazil, with a description of a new (Sternorrhyncha: Coccoidea: Eriococcidae). Biological species. Lundiana, International Journal of Biodiversity, Journal of the Linnean Society, 83: 441-452. 5: 51-72. Cook, L.G., Gullan, P.J. & Trueman, H.E. 2002. A Kondo, T., Hardy, N., Cook, L. & Gullan, P. 2006. Description preliminary phylogeny of the scale insects (Hemiptera: of two new genera and species of Eriococcidae (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-unit Coccoidea) from southern South America. Zootaxa, 784: ribosomal DNA. Molecular Phylogenetics and Evolution, 1-12. 25: 43-52. Kozár, F. 2009. Zoogeographical analysis and status of González, P. 2009. Eriocóccidos (Hemiptera: Coccoidea) encon- knowledge of the Eriococcidae (Hemiptera), with a world trados en Larrea spp. (Zygophyllaceae) en Argentina. Revista list of species. Bollettino di Zoologia agrarium di de la Sociedad Entomológica Argentina, 68: 115-134. Bachicultura, Ser. II, 41: 87-121.

72 Lundiana 10(1):73-75, 2009 © 2011 Instituto de Ciências Biológicas - UFMG ISSN 1676-6180

SHORT COMMUNICATION Redescoberta de Mackenziaena severa (Lichtenstein, 1823) (Aves: Thamnophilidae) no limite sul de sua distribuição geográfica, Rio Grande do Sul, Brasil

Ismael Franz Comitê Brasileiro de Registros Ornitológicos - CBRO e Laboratório de Zoologia, Centro Universitário Feevale, RS 239, 2755. 93352-000, Novo Hamburgo, RS, Brasil. E-mail: [email protected]

Abstract Rediscovery of Mackenziaena severa (Lichtenstein, 1823) (Aves: Thamnophilidae) at the south limit of its range, state of Rio Grande do Sul, Brazil. In this short note I present records of the Tufted Antshrike, Mackenziaena severa (Lichtenstein, 1823), in a forest fragment located between the municipalities of Campo Bom and Dois Irmãos (29º37’S, 51º03’W), state of Rio Grande do Sul, southern Brazil, close to its previous historical southernmost record (Igrejinha, around 1880). Recent records known for the species in the state (second half of the 20th century) are all from 300 km northwestward. I suggest that the specimens recorded here are part of a small relictual population and do not represent an event of recent re-colonization from other areas.

Keywords: Tufted Antshrike, distribution, relictual population, Atlantic Forest, southern Brazil

Restrita à Mata Atlântica, a borralhara, Mackenziaena severa Todos os novos registros ocorreram em um remanescente (Lichtenstein, 1823), distribui-se atualmente, no Brasil, desde o florestal (29°37’S, 051°03’W) localizado na divisa entre os Espírito Santo e sul de Minas Gerais até o norte do Rio Grande municípios de Campo Bom e Dois Irmãos, na escarpa do Sul, no nordeste da Argentina, na província de Misiones, e no meridional do Planalto. Com aproximadamente 90 ha, o departamento de Alto Paraná, extremo leste do Paraguai fragmento está inserido na região fitoecológica da Floresta (Ridgely & Tudor, 1994; Sick, 1997). No Rio Grande do Sul, a Estacional Semidecidual Submontana, entre o extremo leste da espécie é atualmente conhecida apenas em áreas de florestas Depressão Central Gaúcha e os patamares da Serra Geral, na estacionais no extremo noroeste do estado, mais precisamente no bacia do Rio dos Sinos (Teixeira et al., 1986), a 90 m de Parque Estadual do Turvo (município de Derrubadas), na Terra altitude. A floresta apresenta-se em estádio médio a avançado de Indígena de Nonoai/Rio da Várzea e no Parque Municipal de sucessão (no presente, são raros os agrupamentos florestais Iraí. Contudo, há um registro histórico para a escarpa sudeste do originais nesta região que, ao longo da colonização européia, foi Planalto Meridional, no leste do estado, onde um espécime foi intensamente desmatada para fins agrícolas, industriais e coletado por Theodor Bischoffi, por volta de 1880, em Picada urbanos) e é circundada por diversos fragmentos de diferentes Arroio Grande, que atualmente corresponde à localidade de dimensões e graus de degradação e uso, em uma paisagem Solitária, município de Igrejinha (Berlepsch & Ihering, 1885; altamente fragmentada. Belton, 1985; 1994; Bencke et al., 2003). Este registro é o mais A borralhara foi registrada em quatro ocasiões. No dia 9 de meridional conhecido para a espécie. março de 2005, por volta das 10:00 h, um macho foi visto no Segundo Bencke et al. (2003), a borralhara estaria extinta na local pela primeira vez, no interior da floresta, no estrato baixo escarpa do Planalto, pois não existem registros nessa região há da vegetação (~1,5 m do solo). O indivíduo não vocalizou e mais de 100 anos. Aqui são apresentados novos registros para as permaneceu no local por cerca de 4 min. Em 2 de maio de 2005, proximidades do local de ocorrência histórica de M. severa no um macho foi atraído com o uso de playback no mesmo local do leste do Rio Grande do Sul. primeiro registro. Ele não emitiu qualquer tipo de vocalização durante os cerca de 10 min em que se deslocou pelo local. Voava sempre baixo, chegando a se aproximar a cerca de 1 m do Received: 18-VII-08 observador. Na ocasião, foi observado se alimentando de Accepted: 30-VII-09 formigas voadoras (Hymenoptera: Formicidae). A ave afastou-se Distributed: 13-IX-11 e, após aproximadamente 30 min, começou a vocalizar a cerca

73 Franz

de 100 m de distância do observador. Em expedições posteriores altura, estratos inferior e médio densos (com adensamentos ao local (em fevereiro, março, abril e maio de 2006 e em esparsos de bambus [Merostachys sp.]), luminosidade reduzida e fevereiro de 2007) a espécie não foi reencontrada. Em 8 de declividade acentuada. março de 2007, vocalização da espécie foi escutada às 17:00 h, O local dos novos registros dista 300 km em linha reta das muito distante. Na manhã seguinte, uma gravação da voz foi áreas de ocorrência conhecida no extremo noroeste do estado obtida (cópia depositada na Coleção de Sons da Universidade (Fig. 1) e representa o ponto mais meridional em que a espécie Estadual de Londrina – CSUEL, código ISF 01/001) e, com o já foi registrada, consistindo, possivelmente, no limite sul de sua uso de playback, um macho foi novamente atraído. Ele se distribuição. Como não são conhecidos registros entre essas duas deslocava pelo estrato inferior, entre emaranhados de cipós e regiões, é possível que os indivíduos encontrados pertençam a galhos, sem se aproximar. Às 16:00 h do mesmo dia, dois uma pequena população relictual e não representem um evento indivíduos vocalizaram simultaneamente na mesma área do de recolonização a partir de outras regiões. Corrobora esta fragmento (~3 ha) em que todos os registros ocorreram. Essa hipótese o fato de que aves da família Thamnophilidae área é caracterizada por apresentar dossel com cerca de 9 m de geralmente são sedentárias, com capacidade limitada de

Figura 1 - Locais de ocorrência de Mackenziaena severa (Lichtenstein, 1823) no estado do Rio Grande do Sul, Brasil. Fontes das coordenadas geográficas: pontos 1, 2 e 3 (círculos) - banco de dados do projeto “Livro Vermelho da Fauna Ameaçada de Extinção no Rio Grande do Sul” (Bencke et al., 2003); Igrejinha - coordenada central do município.

74 Redescoberta de Mackenziaena severa

dispersão por áreas abertas (Zimmer & Isler, 2003). Belton, W. 1994. Aves do Rio Grande do Sul, distribuição e Outros fragmentos florestais, próximos ou contíguos a esse, biologia. São Leopoldo, Ed. Unisinos, 584 pp. devem ser amostrados com o objetivo de se localizar novos Bencke, G. A.; Fontana, C. S.; Dias, R. A.; Maurício, G. N. & indivíduos de M. severa. Contudo, a espécie pode ser Mähler Jr., J. K. F. 2003. Aves. In: Fontana, C. S.; Bencke, considerada rara na região e, aparentemente, com densidade G. A. & Reis, R. E. (Orgs.) Livro vermelho da fauna populacional muito baixa. Sugiro, portanto, que o seu atual ameaçada de extinção no Rio Grande do Sul. Porto status de conservação no Rio Grande do Sul (“Criticamente em Alegre, EDIPUCRS, pp. 189-479. Perigo”) seja mantido, apesar dos novos registros apresentados. Berlepsch, H. von & Ihering, H. von 1885. Die vögel der Agradecimentos umgegend von Taquara do Mundo Novo, Prov. Rio Grande do Sul. Ornis - Zeitschrift für die gesammte Ao Glayson Ariel Bencke, Rafael Antunes Dias, Jan Karel Ornithologie: 1-88. Felix Mahler Junior e Giovanni Nachtigall Maurício pelas Ridgely, R. S. & Tudor, G. 1994. The birds of South importantes sugestões ao manuscrito e produtivas discussões. America: The Suboscine Passerines. Vol. 2. Austin, Ao Marcelo Ferreira de Vasconcelos pela revisão do texto e University of Texas Press, 940 pp. pelas sugestões. Ao Jeremy Minns por ceder uma gravação da borralhara. Ao Dr. Luiz dos Anjos pelo tombamento da gravação Sick, H. 1997. Ornitologia brasileira. Rio de Janeiro, Nova na Coleção de Sons da Universidade Estadual de Londrina Fronteira, 912 pp. (CSUEL), Laboratório de Ornitologia e Bioacústica. Ao Bráulio Teixeira, M. B.; Coura Neto, A. B.; Pastore, U. & Rangel- Blos e sua família pela acolhida e por autorizarem as pesquisas Filho, A. L. R. 1986. Vegetação. In: IBGE. Levantamento em sua propriedade. de recursos naturais. Vol. 33. Rio de Janeiro, IBGE, pp. 541-620. Zimmer, K. J. & Isler, M. L. 2003. Family Thamnophilidae Referências (Typical Antbirds). In: del Hoyo, J.; Eliott, A. & Sargatal, J. Belton, W. 1985. Birds of Rio Grande do Sul, Brazil. Part 2: (Eds.) Handbook of the birds of the world. Vol. 8. Formicariidae through Corvidae. Bulletin of the American Broadbills to Tapaculos. Barcelona, Lynx Edicions, pp. 448- Museum of Natural History, 180: 1-242. 681.

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SHORT COMMUNICATION Nesting of the Common Potoo, Nyctibius griseus (Gmelin, 1789) (Aves: Nyctibiidae) in an urban environment in central Cerrado

Luiz Gonzaga A. Mendonça1, Daniel Blamires2 & Dárius P. Tubelis3 1 Universidade Estadual de Goiás, Unidade Universitária de Palmeiras de Goiás. Rua S-7, S/N, Setor Sul, 76190-000, Palmeiras de Goiás, Goiás, Brazil. E-mail: [email protected] 2 Universidade Estadual de Goiás, Unidade Universitária de Iporá. Avenida R-02, Q. 01, Jardim Novo Horizonte, 76200-000, Iporá, GO, Brasil. E-mail: [email protected] 3 Departamento de Ecologia, Universidade de São Paulo, 05508-900, São Paulo, São Paulo, Brazil. E-mail: [email protected]

Abstract This is a report on two nesting attempts by the Common Potoo (Nyctibius griseus) in an urban environment at Palmeiras de Goiás, Goias state, central Brazil. In December 12, 2006, a nest was found on a tree (Caesalpinia pothoroides), 2.8 m above the ground. This nest contained a white egg with dark red and brown patches. A few days later, no eggs were found in this nest. Other nesting attempt was recorded on October 9, 2007, when a chick was found in the same place used as nesting site in 2006. The young was not found in the next days. Our study is the first to document the nesting of N. griseus in the Cerrado core area.

Key words: Caprimulgiformes, nest site, Cerrado, urban ecology.

Potoos (Nyctibiidae) are nocturnal and cryptic birds endemic and Venezuela (Skutch, 1970; Tate, 1994; Greeney et al., 2004), to the Neotropical region (Sick, 1997). The seven species inhabit and few studies were developed in Brazil. For example, Goeldi mainly forests, where they spend the day perched on broken (1896) described its nest in forests of Rio de Janeiro. A more trunks or branches keeping a vertical posture (Cohn-Haft 1999). detailed description of its breeding habits involved observations They most often feed on flying insects during the crepuscular on two nests in a University campus in southern Brazil (Lopes & period or at night (Cohn-Haft 1999). Potoos are monogamous Anjos, 2005). As a result of the scarcity of studies, the breeding birds that nest on tree depressions to which they add no nesting biology of N. griseus remains little or not known in several material (Vanderwerf, 1988; Sick, 1997; Cohn-Haft, 1999; Neotropical regions, including the Cerrado. Lopes & Anjos, 2005). This study reports on two nesting attempts by N. griseus in The Common Potoo (Nyctibius griseus) is widely distributed the urban environment of Palmeiras de Goiás (16º52’30” S; throughout most of the Neotropics (Sick, 1997; Sigrist, 2006). It 49°52’30” W; at an altitude of 600 m), central Goiás state, can be found in a wide range of habitats such as woodlands, Brazil, in the core area of the Cerrado domain (Brazilian savannas, secondary forests and mangroves (Sick, 1997; Cohn- savanna). This municipality harbors about 21,000 people within Haft, 1999; Cooper & Kay, 2004). Camouflage and behavior are an area of 1,540 km² (IBGE, 2007), and is located 79 km from similar to those of other species of the family (Tate, 1994; Cohn- Goiânia (the state capital). The original landscapes around the Haft, 1999). Despite being considered a common species, with city were typical of the Cerrado region (Eiten, 1972; Oliveira & low sensitivity to human disturbance, its biology remains poorly Marquis, 2002), with grasslands and savanna woodlands known (Tate, 1994; Stotz et al., 1996, Cohn-Haft, 1999). dominating uplands, and gallery forests, marshes and veredas The breeding biology of N. griseus has been examined in occurring in the valleys. Due to intense agriculture and wood detail in a few countries, such as Costa Rica, Ecuador, Mexico extraction in the last years, Palmeiras de Goiás is now surrounded by soybean, corn and eucalypt plantations. Remnants of forest and non-forest native vegetation are embedded within these exotic-vegetation matrix. The regional climate is tropical and marked by two well defined seasons – Received: 04-II-08 Accepted: 18-VIII-09 wet and dry (Assad, 1994). Most of the annual precipitation Distributed: 13-IX-11 (1,200 mm to 2,000 mm) falls between October and March. The

77 Mendonça et al.

Figure 1 - Nest of Nyctibius griseus with an egg in the urban zone of Palmeiras de Goiás, central Brazil, in mid December 2006.

dry season occur between May and September. June and July are The nest was 2.8 m above the ground, higher than nests the coldest months, while higher temperatures occur between reported in Goeldi (1896), but lower than nests found in other December and February (Assad, 1994).The neighborhood where studies (Müir & Butler 1925, Skutch 1970, Borrero 1970, 1980, the nesting tree was located was composed of residences and Tate 1994, Lopes & Anjos 2005). The nest cavity, nearly round, commercial buildings. Most streets are paved and car traffic can was close to the major trunk of the tree (Fig. 1), formed by the be intense. Observations on both nests occurred every 2-3 days decomposition of the interior of the basal portion of a broken until the nest content (egg or chick) disappeared. branch. This is a nest of the “simple/unlined type” of the First nesting attempt. A nest of N. griseus was found on a “elementary standard” of Simon & Pacheco’s (2005) tree (Caesalpinia pothoroides, Fabaceae), in December 12, classification; narrower (33 mm in diameter) than those of nest 2006. On the occasion, an adult was on the nest, its vertical cavities described previously (Goeldi, 1896; Müir & Butler, posture making it resemble the apex of a broken branch, as 1925; Borrero, 1970; Lopes & Anjos, 2005), and with a depth described previously (Tate, 1994; Cohn-Haft, 1999; Sick, 1997; (22 mm deep) comparable to those of nests found in southern Lopes & Anjos, 2005; Sigrist, 2006). The nesting tree was Brazil (Lopes & Anjos, 2005). adjacent to other four trees, forming a continuous canopy. The nest had only one white egg, with dark red and brown Around this group of trees, shrubs were absent and grasses patches concentrated on its equator and large pole as described occurred as isolated patches. The nesting tree was on the in previous studies examining the reproduction of N. griseus in walking side of a paved road with intermediate car traffic. other regions (Cohn-Haft, 1999; Cooper & Kay, 2004; Lopes &

78 Nesting of the Common Potoo, Nyctibius griseus (Gmelin, 1789) (Aves: Nyctibiidae) in an urban environment in central Cerrado

Anjos, 2005). No material was found in the nest, in agreement References with findings of potoo nests elsewhere (Goeldi, 1896; Müir & Butler, 1925; Skutch, 1970; Borrero, 1980; Tate, 1994; Cohn- Assad, E. D. 1994. Chuva nos cerrados. Análise e Haft, 1999; Lopes & Anjos, 2005). Also, no feces were found Espacialização. Embrapa/SPI, Brasília, 423 pp. inside or below the nest, similarly to reports by Skutch (1970) Borrero, J. L. 1970. Photographic study of the potoo in and Lopes & Anjos (2005). This clean aspect probably reduces Colômbia. Living Bird, 9: 257-263. the probability of nest finding by predators, as suggested for Borrero, J. L. 1980. Notas sobre el comportamiento del Perico birds in general (Sick 1997). de Pluma (Nyctibius griseus). Lozania, 32: 1-6. Second nesting attempt. In December 9, 2007, an adult and a chick were found on the same cavity used as nesting site in the Cohn-Haft, M. 1999. Family Nyctibiidae (potoos). In: del previous year. The adult was partially covering the chick with its Hoyo, J.; Elliot, A. & Sargatal, J. (Ed.). Handbook of the abdominal feathers. Both the adult and young were in vertical Birds of the World. Vol. 5: Barn-owls to Hummingbirds. position, as reported previously for this species (Tate, 1994; Barcelona, Lynx Edicions. pp. 288-301 Cohn-Haft, 1999; Lopes & Anjos, 2005). The chick was totally Cooper, D. & Kay, B. 2004. Common Potoo Nyctibius griseus. covered by white down, as reported for recently-born youngsters Cotinga, 22: 95-96. (Lopes & Anjos, 2005). On few occasions, the adult adjusted its Eiten, G. 1972. The cerrado vegetation of Brazil. Botanical position on the nest, trying to hide the young. As occurred in the Review, 38: 205-341. previous nesting attempt, no feces or nesting materials were found on the nest or in the tree surroundings. Goeldi, E. A. 1896. Sobre a nidificação do Nyctibius jamaicensis, The last months of the year are usually marked by both high Urutáo e Sclerurus umbretta, Vira-Folha. Ibis, 7: 210-217. temperatures and precipitation in the study area (Assad, 1994). Greeney, H. F.; Gelis, R. A. & White, R. 2004. Notes on the During this period, artificial lights in the city attract high breeding birds from an Ecuadorian lowland forest. Bulletin quantities of insects (L. G. A. M., pers. obs.). Thus, the nesting of the British Ornithologist’s Club, 124: 28-37. period of N. griseus at Palmeiras de Goiás appears to occur IBGE. 2007. Cidades. Rio de Janeiro. Fundação Instituto during high food availability. According to Cohn-Haft (1999), Brasileiro de Geografia e Estatística. Website: http:// the breeding activities of potoos may be restricted to a short www.ibge.gov.br/cidadesat/default.php period in some localities. Our findings are in agreement with Tate (1994), who recorded the reproduction of N. griseus during Lopes, E. V. & Anjos, L. C. 2005. Observações sobre a the rainy season in central Venezuela, and with Lopes & Anjos reprodução de Nyctibius griseus no campus da Universidade (2005), who found two nests of N. griseus during a rainy, warm Estadual de Londrina, norte do Paraná. Ararajuba, 13: 109- period in southern Brazil. 112. Consecutive visits to the nesting tree revealed the Muir, A. & Butler, A. L. 1925. The nesting of Nyctibius development of the breeding attempts. In January 8, 2007, after griseus (Gmel.) in Trinidad with photographs by Alec Muir, the first nesting attempt, no eggs were found in the nest. and some remarks by A. L. Butler. Ibis, 12: 654-659. Detailed search in the surroundings of the tree did not result in Oliveira, P. S. & Marquis, R. J. 2002. The Cerrados of Brazil. the finding of egg pieces or of the young and it was concluded Ecology and Natural History of a Neotropical Savanna. that the nest was preyed. On the other hand, the young produced New York, Columbia University, 398 pp. in the second nesting attempt could be followed for more than 10 months, but was not seen in the nest after October 28, 2008. Sick, H. 1997. Ornitologia Brasileira. Rio de Janeiro, Nova In the last visit it was found on the nest, it was nearly the size of Fronteira, 862 pp. an adult, and most of its cover and flight feathers were Sigrist, T. 2006. Aves do Brasil. Uma Visão Artística. Birds developed. We are unsure about the success of this breeding of Brazil. An artistic view. São Paulo, Fosfertil, 672 pp. attempt, as this young potoo could have flown out of the nest or Silva, J. M. C. 1995. Birds of the Cerrado region, South been preyed. Although N. griseus may find suitable conditions America. Steenstrupia, 21: 69–92. for reproduction (insects and nesting trees) in urban environments, their nesting success may be threatened. We Simon, J. E. & Pacheco, S. 2005. On the standardization of suggest that the most likely nest predators in the study area are nest description of neotropical birds. Revista Brasileira de people and domestic cats. Our study is the first to document the Ornitologia, 13: 143-154. nesting of N. griseus in the Cerrado core area, although these Skutch, A. 1970. Life history of the Common Potoo. Living records were done in an urban environment. Studies conducted Bird, 9: 265-280. in Cerrado natural landscapes are still needed for the Stotz, D. F.; Fitzpatrick, J. W.; Parker III, T. A. & Moskovits, understanding of the common potoo reproduction in Central D. K. 1996. Neotropical Birds: Ecology and Conser- Brazil. vation. Chicago, University of Chicago, 478 pp. Acknowledgements Tate, D. P. 1994. Observations on nesting behavior of the Common Potoo in Venezuela. Journal of Field Orni- We thank Rafael Gonçalves de Sousa for important help thology, 65: 447-452. during field work. Dr. José Hidasi (Fundação Museu de Vanderwerf, E. A. 1988. Observations on the nesting of the Ornitologia de Goiânia) provided important assistance. D. P. Great Potoo (Nyctibius grandis) in central Venezuela. Tubelis thanks FAPESP for support during part of this study. Condor, 90: 948-950.

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