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New findings of phytophagous insects (Hemiptera: Coccoidea and Aphidoidea) from Ilhéu Chão (Desertas Islands, Madeira Archipelago)

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Here we report new taxonomic findings of aphids (Aphidoidea) and scales (Coccoidea) for Ilhéu Chão (Desertas Islands, Madeira Archipelago). Protaphis pseudocardui (Theobald, 1915) is for the first time reported to Madeira archipelago while the aphids Aphis craccivora, A. gossypii, A. umbrella and Uroleucon sonchi, and the scales Coccus cf. hesperidum, Icerya purchasi, Pulvinaria urbicola, Saissetia coffeae and S. oleae are new findings to the Desertas Islands. We also provide information on the host plant associations of these phytophagous insects. Our results highlight the need for further research on the insect fauna of Desertas Islands. No. LXVIII, Art. 351 26
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BOLETIM
MUSEU DE
HISTÓRIA NATURAL DO FUNCHAL
Vol. LXVIII (2018), Art. 351: 25-30
Received: 23 August 2018; Available online: 31 December 2018; Published: 31 December 2018
New ndings of phytophagous insects
(Hemiptera: Coccoidea and Aphidoidea)
from Ilhéu Chão (Desertas Islands, Madeira Archipelago)
By Cândida Ramos
1 *
, a. m. FRanqui nho aguiaR
2
, isamBeRto silva
3
, ana mouRão
1
, Renata santos
4
, CaRla Rego
4
& máRio BoieiRo
4
With 6 gures
1 Departament of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, 4169-007 Porto, Portugal.
* Corresponding author: candidasgramos29@gmail.com
2 Entomology Lab, Laboratório de Qualidade Agrícola, Secretaria Regional de Agricultura e Pescas, Caminho Municipal dos Caboucos, 61, 9135-372
Camacha, Madeira, Portugal.
3 Instituto das Florestas e da Conservação da Natureza, Quinta do Bom Sucesso, Caminho do Meio, 9050-251 Funchal, Madeira, Portugal.
4 Centre for Ecology, Evolution and Environmental Changes (cE3c), Azorean Biodiversity Group and Department of Environmental Sciences and
Engineering, University of the Azores, 9700- 042 Angra do Heroísmo, Azores, Portugal.
ABSTRACT: Here we report new taxonomic ndings of aphids (Aphidoidea) and scales (Coccoidea) for Ilhéu Chão
(Desertas Islands, Madeira Archipelago). Protaphis pseudocardui (Theobald, 1915) is for the rst time reported to
Madeira archipelago while the aphids Aphis craccivora, A. gossypii, A. umbrella and Uroleucon sonchi, and the scales
Coccus c f. hesperidum, Icerya pu rchasi, Pulvinaria urbicola, Saissetia coeae and S. oleae are new ndings to the Desertas
Islands. We also provide information on the host plant associations of these phytophagous insects. Our results
highlight the need for further research on the insect fauna of Desertas Islands.
Keywords: faunistic records, host plant associations, aphids, scales, Protaphis pseudocardui, Ilhéu Chão, Desertas
Islands, Madeira Archipelago.
Boletim do Museu de História Natural do Funchal No. LXVIII, Art. 35126
RESUMO: Neste artigo reportamos novas descobertas taxonómicas de afídeos (Aphidoidea) e cochonilhas
(Coccoidea) para o Ilhéu Chão (Ilhas Desertas, Arquipélago da Madeira). A presença de Protaphis pseudocardui
(Theobald, 1915) é pela primeira vez relatada no arquipélago da Madeira, enquanto que os afídeos Aphis craccivora,
A. gossypii, A. umbrella e Uroleucon sonchi, e as cochonilhas Coccus cf. hesperidum, Icerya purchasi, Pulvinaria urbicola,
Saissetia coeae e S. oleae, são novas descobertas para as Ilhas Desertas. Também fornecemos informações sobre as
associações destes insetos tófagos com as plantas hospedeiras. Os nossos resultados salientam a necessidade de
mais estudos sobre a fauna de insetos das Ilhas Desertas.
Palavras-chave: registos faunísticos, associações de plantas hospedeiras, afídeos, cochonilhas, Protaphis
pseudocardui, Ilhéu Chão, Ilhas Desertas, arquipélago da Madeira.
INTRODUCTION
Phytophagous insects are one of the most speciose
groups of living organisms worldwide being also well
represented on oceanic islands. In many archipelagos,
they are an important fraction of the overall biodiversity
and include a high number of endemics and remarkable
examples of species diversication and ecological
associations (
Borges
et al., 2008a;
Percy
, 2010;
Machado
et al.,
2017). Besides their ecological importance in most natural
terrestrial habitats (
olff
&
ritchie
, 1998;
Belovsky & slade
,
2000), phytophagous insects also have a prominent role
in human-changed habitats, particularly in forestry and
agricultural elds, due to their direct and indirect impacts
on the production of goods for human consumption.
The dramatic increase in the transportation of goods and
commodities during the last decades contributed to the
introduction of many phytophagous insect species in
island ecosystems, where some have been responsible for
huge economic losses, negative social impacts and severe
consequences for the conservation of native biodiversity
(
PoMBo
et al., 2010).
The species checklist of Madeira and Selvagens
archipelagos was a major landmark for the knowledge
of the biodiversity of these islands by providing updated
information on species taxonomy and distribution
for most groups of living organisms, including all
phytophagous insects groups (
Borges
et al., 2008b). Two
recent works updated the information on the scales
(Coccoidea) and aphid species (Aphidoidea) from Madeira
archipelago, which now comprehend respectively 109
and 183 species (
franco
et al., 2011;
aguiar
et al., 2013).
However, the knowledge on the phytophagous insects of
Madeira is far from being complete since new taxonomic
ndings are still occurring (
aguiar & ilharco
, 2005) and basic
information on abundance, distribution and host plant
associations is lacking for most species. The aim of this
study is to present new ndings of scales and aphids from
Ilhéu Chão (Desertas Islands) jointly with information on
species distribution and their association with host plants.
MATERIAL AND METHODS
The studied specimens were collected at Ilhéu Chão,
in Desertas Islands, between 19 and 22 of June 2017. Ilhéu
Chão is the smallest of the three Desertas Islands with 1km2
and presents a relatively well-preserved plant cover with
several vegetation patches dominated by native species
(e.g. Artemisia argentea, Asphodelus stulosus, Jasminum
odoratissimum, Suaeda vera) (
Menezes
et al., 2005). The insects
were collected from several plant species (see RESULTS
AND DISCUSSION section) and were frequently found in
association with the invasive Argentine ant (Linepithema
humile) (
raMos
, 2017). All specimens were captured with
the aid of forceps and stored in vials in 70% ethanol. Later,
they were identied using a stereomicroscope (Nikon
Optiphot-2) and specic literature (
BlackMan & eastoP
, 1989;
1994; 2006;
nieto nafría
et al., 2004;
BlackMan
, 2013), at the
Laboratório de Qualidade Agrícola (LQA) and have been
deposited in the entomological collection (ICLAM) of this
institution preserved in 70% ethanol or slide-mounted.
Below we present our ndings jointly with information
on sampling dates, site location, species associations and
photographs of some species. The family and species-
names are listed alphabetically following
Borges
et al.
(2008b) and ecological and distributional information is
presented for each species. The collection code is also
indicated for the specimens stored in ICLAM.
RESULTS AND DISCUSSION
Overall, many specimens from 12 phytophagous
insect species were collected in this study (see below).
Six species are scales (Coccoidea) and the other six aphids
Ramos et al., New nding of phytophagous insects from Desertas Islands2018 27
(Aphidoidea). All scale (except Hemiberlesia lataniae) and
aphid species are new ndings to Desertas Islands and the
aphid Protaphis pseudocardui (Theobald, 1915) is recorded
for the rst time in the archipelago. Comprehensive data
on the sampled species is presented below.
Superfamily Coccoidea
Family Coccidae
Coccus cf. hesperidum Linnaeus, 1758
Material examined: Ilhéu Chão, 21/06/2017, 1
immature (ICLAM: C1251).
Remarks: Coccus hesperidum was previously known
from Madeira and Porto Santo while its congener C. viridis
Green, 1889 is restricted to Madeira Island (
aguiar
, 2008).
We found a single specimen matching the description of
C. hesperidum associated with the endemic plant Artemisia
argentea (Asteraceae).
Pulvinaria urbicola Cockerell, 1893
Material examined: Ilhéu Chão, 21/06/2017, 28 ♀♀
(ICLAM: C1259, C1267, C1269, C1272).
Remarks: This native species was previously known
from Madeira Island (as Pulvinaria grabhami a junior
synonym of P. urbicola) (
aguiar
, 2008). In Ilhéu Chão, the
species was found in association with the native plants
Plantago coronopus (Plantaginaceae), Silene uniora
(Cariophyllaceae) and the endemic Artemisia arg entea (Fig. 1).
Fig. 1Pulvinaria urbicola adult females in association with
Artemisia argentea. Photo credit: Cândida Ramos.
Saissetia coeae (Walker, 1852)
Material examined: Ilhéu Chão, 19/06/2017, many
immature and adult ♀♀ (ICLAM: C1255).
Remarks: This introduced species was previously
known from Madeira and Porto Santo Islands (
aguiar
,
2008). Now, it was found in Ilhéu Chão in association with
Silene sp. (Cariophyllaceae).
Saissetia oleae (Olivier, 1791)
Material examined: Ilhéu Chão, 21/06/2017, many
immature and adult ♀♀ (ICLAM: C1252, C1268, C1270).
Remarks: This introduced species was reported from
Madeira and Porto Santo Islands (
aguiar
, 2008). At Ilhéu
Chão, we found it in association with the endemic plants
Artemisia argentea and Phagnalon lowei (Asteraceae).
Family Diaspididae
Hemiberlesia lataniae (Signoret, 1869)
Material examined: Ilhéu Chão, 21/06/2017, many
adult ♀♀ (ICLAM: C1250, C1254, C1256, C1268a).
Remarks: This native species was known from
Madeira, Porto Santo and Desertas Islands (
aguiar
, 2008).
In this study it was found in association with the endemic
plants Artemisia argentea and Phagnalon lowei.
Family Monophlebidae
Icerya purchasi Maskell, 1879
Material examined: Ilhéu Chão, 21-22/06/2017, many
immature and adult ♀♀ (ICLAM: C1249, C1253, C1257,
C1260, C1271).
Remarks: This introduced species was only known
to occur in Madeira (
aguiar
, 2008). It was now found in
Ilhéu Chão, in association with Artemisia argentea (Fig. 2)
and Sonchus oleraceus (Asteraceae).
Fig. 2Icer ya purchasi adult females in association with Ar temisia
argentea. Photo credit: Cândida Ramos.
Boletim do Museu de História Natural do Funchal No. LXVIII, Art. 35128
Superfamily Aphidoidea
Family Aphididae
Aphis craccivora Koch, 1854
Material examined: Ilhéu Chão, 22/06/2017, 5
apterous ♀♀ (ICLAM: A1157).
Remarks: This native species was known from
Madeira and Selvagens (
aguiar & ilharco
, 2008) and was
now found in Ilhéu Chão associated with Silene sp.
Aphis gossypii Glover, 1877
Material examined: Ilhéu Chão, 21/06/2017, 12
apterous ♀♀ (ICLAM: A1162).
Remarks: This native species had been reported
from Madeira and Porto Santo Islands (
aguiar & ilharco
,
2008). It was now found in Ilhéu Chão associated with the
endemic plant Crepis divaricata (Asteraceae) (Fig. 3).
Fig. 3Aphis gossypii adult females on Crepis divaricata. Photo
credit: Cândida Ramos.
Protaphis pseudocardui (Theobald, 1915)
Material examined: Ilhéu Chão, 21/06/2017, 4
alate and 8 apterous ♀♀ (ICLAM: A1161).
Remarks: This is the rst record of this species in
Madeira Archipelago. Protaphis pseudocardui was found in
association with an unidentied Asteraceae.
Aphis umbrella (Börner, 1950)
Material examined: Ilhéu Chão, 21/06/2017, 5 alate
and 4 apterous ♀♀ (ICLAM: A1158).
Remarks: This native species was known from
Madeira Island (
aguiar & ilharco
, 2008). We found it in Ilhéu
Chão associated with the native plant Lavatera cretica
(Malvaceae) (Fig. 4).
Fig. 4Aphis umbrella adult females on the underside of a
Lavatera cretica leaf, being tended by a worker of the invasive
Argentine ant Linepithema humile. Photo credit: Cândida Ramos.
Fig. 5Macrosiphoniella sp. adult females on Artemisia argentea
leaves. Photo credit: Cândida Ramos.
Macrosiphoniella sp.
Material examined: Ilhéu Chão, 22/06/2017, 1 nymph
and 1 apterous (ICLAM: A1159).
Remarks: This genus is known from Madeira and
Porto Santo Islands. Besides the Madeiran endemic
Macrosiphoniella madeirensis (
aguiar & ilharco
, 2005), four
other introduced species are also known to occur in the
archipelago – M. artemisiae (Fonscolombe, 1841), M.
millefolii (De Geer, 1773), M. sanborni (Gillette, 1908) and
M. tapuskae (Hottes & Frison, 1931) (
aguiar & ilharco
, 2008).
We found two specimens of this genus in Ilhéu Chão in
association with Artemisia argentea (Fig. 5). It was not
possible to identify the species with condence since
both specimens were in bad condition. However, they are
most probably M. artemisiae since this species is known to
associate with Artemisia argentea in Madeira.
Uroleucon sonchi (Linnaeus, 1767)
Material examined: Ilhéu Chão, 21/06/2017, many
nymphs and apterous ♀♀ (ICLAM: A1160).
Ramos et al., New nding of phytophagous insects from Desertas Islands2018 29
Remarks: This native species was known from
Madeira and Porto Santo Islands, but also from Selvagens
Archipelago (
aguiar & ilharco
, 2008). We found it in Ilhéu
Chão associated with Sonchus oleraceus (Fig. 6).
Fig. 6Uroleucon sonchi adult females on Sonchus oleraceus.
Photo credit: Cândida Ramos.
Our ndings considerably increase the knowledge
on the scales and aphids from Desertas. The species
checklist of these islands is updated and now includes 8
scale (Coccoidea) and 12 aphid species (Aphidoidea). The
discovery of the aphid Protaphis pseudocardui (Theobald,
1915), a hitherto unknown species in the archipelago, was
unexpected and highlights the need for further studies to
survey the insect biodiversity of Desertas. These surveys
should be carried in all three Desertas Islands since
they have been poorly sampled and their dierences
in geomorphology and historical legacy may translate
in distinct taxonomic assemblages. The ecological
information on scales and aphids showed that many
species feed on the endemic Artemisia argentea, which
seems to be a key host plant at Ilhéu Chão by supporting
large populations of dierent phytophagous species. On
the other hand, some phytophagous insects, particularly
aphids, were found associated to a single host plant,
which may render them more vulnerable to ecological
disturbances in the simplied ecosystem of Ilhéu Chão.
The scales and aphids are engaged in mutualistic
interactions with the invasive Argentine ant, beneting of
protection from predators and parasitoids and providing
a rich food resource (the honeydew) to these aggressive
ants. The consequences of these associations (frequently
involving a pair of exotic species) on the natural
communities of Ilhéu Chão remain unstudied but may
negatively aect native species survival and the structure
of natural assemblages.
ACKNOWLEDGEMENTS
This study was funded through projects PTDC/BIA-
BIC/1013/2014 by Fundação para a Ciência e a Tecnologia
(FCT, Portugal) and LIFE Recover Natura (LIFE12/NAT/
PT/000195) by the European Regional Development Fund.
MB and CR were supported by FCT grants (respectively
SFRH/BPD/86215/2012 and SFRH/BPD/91357/2012). We
also thank Instituto das Florestas e da Conservação da
Natureza (IFCN) for logistical support and permission to
collect insects in Desertas Nature Reserve.
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A first comprehensive checklist of the scale insects of Portugal, including Azores and Madeira Archipelagos, is presented comprising a total of 168 species: 124 from Mainland, 109 from Madeira, and 52 from Azores. The listed species are distributed among 85 genera and 15 families.
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Provides a comprehensive species-by-species account of all the world's tree-dwelling aphids (1758 species). An introductory section gives notes on aphid life cycles, polymorphism and the association between aphids and trees. The second section begins with information on morphology and key characters, a list of the plant families with tree genera from which aphids are recorded is then provided. Host lists and keys for each tree genus make up the bulk of this section. The section concludes with a key to the 23 species of polyphagous aphids which are found on various tree genera. Secion three contains information on the aphids listed and keyed in the previous section, comprising: appearance in life; body length of one or more morphs; host plants; distribution; life cycle, including time of appearance of sexual morphs if known; parasitoids; references to the biology and economic importance; and chromosome number where known. Section four consists of a brief coverage of techniques: collecting; preservation and mounting; and labelling and storage. Thirty-seven pages of references are included in the bibliography. The volume concludes with a collection of photographs of slide-mounted aphids. -S.R.Harris
Insect herbivory accelerates nutrient cycling and increases plant production
  • G E J B Belovsky
  • Slade
BELOVSKY, G. E. & J. B. SLADE: 2000. Insect herbivory accelerates nutrient cycling and increases plant production. Proceedings of the National Academy of Sciences of the United States of America. 97: 14412-14417.
Aphids on the world's plants -an online identification and information guide
  • R L Blackman
BLACKMAN, R. L.: 2013. Aphids on the world's plants -an online identification and information guide.
Fauna Europaea: Hemiptera, Aphidoidea, Fauna Europaea version 1.0
  • J M Nieto Nafría
NIETO NAFRÍA, J. M.: 2004. Fauna Europaea: Hemiptera, Aphidoidea, Fauna Europaea version 1.0, 27 September 2004. http://www.faunaeur.org [accessed 07/06/2017].