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Establishment and new hosts of the non-native seed beetle Stator limbatus (Coleoptera, Chrysomelidae, Bruchinae) on acacias in Europe
expand article infoArturo Cocco, Giuseppe Brundu, Cyril Berquier§|, Marie Cécile Andreï-Ruiz§|, Michelina Pusceddu, Marco Porceddu, Lina Podda, Alberto Satta, Yohan Petit#|, Ignazio Floris
‡ University of Sassari, Sassari, Italy
§ Observatoire Conservatoire des Insectes de Corse, Corte, France
| Office de l’Environnement de la Corse, Corte, France
¶ University of Cagliari, Cagliari, Italy
# Conservatoire Botanique National de Corse, Corte, France
Open Access

Abstract

Stator limbatus is a phytophagous beetle native to warm regions of North and Central America, feeding on Fabaceae seeds and one of the most polyphagous species within the subfamily Bruchinae, here reported for the first time in Europe and on new hosts. Adult beetles emerged from Acacia spp. seeds collected in the islands of Corsica (France), and Sardinia (Italy). The wide presence in Sardinia and Corsica supports the hypothesis that this alien species was introduced several years ago. In both islands, S. limbatus emerged from Acacia mearnsii seeds, with infestation rates of up to 74.2 and 90.8% in 2019 and 2020, respectively. This seed beetle also emerged from two previously unreported host species, Acacia saligna and A. pycnantha, showing highest infestation rates of 4.0 and 95.1%, respectively. Both Acacia species are reported as new host associations with S. limbatus. Overall, seed infestation rates recorded in 2019 and 2020 indicate that S. limbatus is well established and that Mediterranean bioclimatic conditions are suitable for its population increase in size. This study lays the foundations for further research on known and potential host species and the spread and distribution of S. limbatus in Europe.

Keywords

Acacia mearnsii, Acacia pycnantha, Acacia saligna, alien species, bean weevil, biological invasion, Mediterranean islands

Introduction

The global movement of people and goods and climate change are dramatically promoting the introduction of alien species in non-native environments in the Anthropocene (Kueffer 2017), resulting in a continuous accumulation of these species worldwide (Seebens et al. 2017; Venette and Hutchison 2021). This indicates that current measures to avoid new introductions of alien species are not always effective. Therefore, prevention, continuous monitoring in priority sites, early detection, and rapid intervention are of major importance for avoiding the establishment of new invasive alien species and agricultural or forestry pests and for reducing the spread of the existing ones, with special concern towards protected areas and natural ecosystems.

Among seed-feeding insects, the subfamily Bruchinae (Coleoptera, Chrysomelidae) beetles, renowned as bean weevils, is highly specific and likely the most important (van Klinken 2005). This family includes about 4,350 taxa distributed worldwide (Borowiec 1987). The beetle Stator limbatus (Horn, 1873) (Coleoptera, Chrysomelidae: Bruchinae) is an endophagous seed feeder of legumes (Fig. 1). Its native range spans from semiarid and xeric regions of southwestern United States and northern Mexico to dry tropical forests of Central America and northern South America. Stator limbatus has a generalist habit and a wide host range, as it has been collected from > 90 host plant species (de Jesús Parra-Gil et al. 2020), including many species of the genus Acacia s.l. In its native range, it affects mostly native species, but also about 20 non-native species (Stillwell et al. 2007). Despite that, host colonization of S. limbatus populations varies greatly among regions, and distinct populations exhibit host specialization at a local scale (Morse and Farrell 2005a, 2005b). Beetle populations are known to express phenotypic plasticity to host species by adapting pre-imaginal development time and body and egg size (Amarillo-Suarez and Fox 2006; Amarillo-Suarez et al. 2017).

Figure 1.

Habitus of adult Stator limbatus A dorsal and B lateral view.

Eggs are oviposited on mature seeds inside of dehiscent or partially dehiscent pods when they are still on the plant (Johnson 1981a; Kingsolver 2004). Females usually lay one egg per seed, and newly hatched larvae burrow into the seed integument beneath the egg, complete their development and pupate inside the same seed. In the case in which seeds are limiting, more eggs are deposited across a seed (Morse and Farrell 2005a). Beetles emerge from seeds as adults, mate and females start ovipositing within 24–48 hours, under laboratory conditions. Adults are facultatively aphagous, as they only require resources acquired during the pre-imaginal stage to complete development and reproduce (e.g. capital breeders) (Stillwell and Fox 2009). The generation time at 28 °C was determined to be 28–30 days (Amarillo-Suarez and Fox 2006).

Several species within the S. limbatus host range, such as Acacia mearnsii De Wild and Acacia saligna (Labill.) H.L.Wendl. native to Australia, have shown in Europe invasive potential and negative impacts on native species, to the extent that containment measures have been implemented (Lowe et al. 2000; European Union 2014; Tozzi et al. 2021). Therefore, monitoring the presence of seed beetles of invasive Acacia spp. in Europe is relevant in the perspective of finding and evaluating potential natural enemies able to slow the expansion and mitigate the adverse impacts of those species. Since Acacia in the broad sense have been grouped into distinct genera, e.g., Mariosousa, Vachellia, and Senegalia, and also other host species in the Leguminosae have been synonymized or renamed, a dedicated study would be required to define the current host range of the bruchid with valid plant names.

Outside its native range, S. limbatus has been reported in Hawaii (Bridwell 1920), South America (Oliveira and Costa 2009; Romero Gomez et al. 2009; Meiado et al. 2013), South Africa (Rink 2013), Iran (Boroumand 2010; Ghahari and Borowiec 2017), and United Arab Emirates (Delobel 2011), whereas reports from Mauritius, Saudi Arabia, Yemen, and Oman were unconfirmed (Rink 2013).

In the framework of an international project assessing the risk of invasion of selected alien species (ALIEM) (Inghilesi et al. 2018), some Acacia spp. seeds were tested in a germination test during which several individuals of S. limbatus adults emerged from seed lots of A. mearnsii seeds collected in Corsica (France) and Sardinia (Italy) in 2018. This insect species has not been yet recorded in Europe, so that new field collections were planned and carried out in 2019 and 2020.

The main aim of the present study was to investigate the establishment of S. limbatus in Sardinia and Corsica according to the traits described by Yus-Ramos et al. (2014) for alien seed beetles, as well as its host association and infestation levels. In addition, a literature search analysis was carried out to provide an updated inventory of host species of S. limbatus with valid names, as understanding and predicting host shifts on other Acacia species is of pivotal importance in order to define its potential distribution in the Mediterranean Basin.

Materials and methods

Literature search analysis

Data sources used for investigating and updating the host range of S. limbatus were retrieved from major online databases, such as Google Scholar, Web of Science, Scopus, CAB abstracts, and ResearchGate. Papers were directly requested to authors and public repositories and libraries whenever inaccessible online. Different combinations of keywords were used in the literature search related to S. limbatus and its host range. Whenever possible, references were cross-checked and duplicates removed, giving priority to older records. Original plant names were collected from each reference, whereas country and locality records were reported whenever available.

Plant names were cross-checked taking into account relevant literature and different on-line databases, in particular Seigler et al. (2006), Kyalangalilwa et al. (2013), The Legume Phylogeny Working Group (LPWG 2017), World Flora Online (WFO) (2020), Plants of the World Online (POWO 2020), BHL (for original protologues), and the International Plant Name Index (IPNI) (2020). To our best knowledge, the accepted nomenclature was followed according to current taxonomic standards.

Seed collection

Legumes and loments (hereafter pods) with seeds of A. mearnsii were manually collected from adult trees naturalized in Corsica and Sardinia in September-November 2019. Seed sampling was carried out in Sardinia within two Special Areas of Conservation (SACs): “Berchida e Bidderosa” (Natura 2000 code ITB020012) (central eastern Sardinia) and “Monte Linas – Marganai” (Natura 2000 code ITB041111) (southwestern Sardinia), where the most important populations of A. mearnsii are located and the species shows clear invasive traits outcompeting with native vegetation. On the other hand, seeds in Corsica were collected along the eastern side of the island (Fig. 2). In Sardinia, seed sampling was extended to other Acacia species, i.e., Acacia pycnantha Benth. and A. saligna, not previously reported as host species but located nearby the sampling sites of A. mearnsii. Following the emergence of S. limbatus adults from all Acacia species sampled in 2019 (See Results), field collection of seeds was repeated in August-early September 2020 on the same species.

Figure 2.

Map of sampling sites of Acacia spp. pods and seeds in Sardinia (Italy) and Corsica (France).

Acacia saligna is a widespread tree species in Corsica and Sardinia (Lozano et al. 2020), in particular along the coast, and severely impacts the characteristics of soils and diversity and structure of the Mediterranean shrublands (Celesti-Grapow et al. 2016; Tozzi et al. 2021). The other two Acacia species, although common, are much less widespread and form dense populations only in a limited number of sites. The width of the sampling site varied widely, ranging from a single tree to tree stands larger than 1,500 m2, as well as the seed production of trees. Therefore, a minimum of 20 pods per tree, representative of seed production, were collected at random from 1–30 randomly-chosen trees. All in all, the sample size ranged from 75 to 8,500 seeds, depending on the width of the sampling site. In fact, seed production was generally very large in all the investigated Acacia spp. in both years and was not a limiting factor in seed sampling.

Seed examination

The collected pods and seeds were stored at laboratory temperature in cardboard envelopes sealed with adhesive tape, to avoid mold development and the escape of tiny seed beetles. Envelopes were opened after approximately three months and beetles were separated and identified morphologically using identification keys for S. limbatus adult detection (Johnson 1963; Kingsolver 2004). Seeds were further inspected under a dissecting microscope and the number of Acacia spp. seeds with emergence holes was determined in order to calculate the rate of infestation. Seeds of A. saligna showed very low seed infestation rates (see Results). However, in view of its importance as an invasive species and in order to point out a potential host shift, the presence of S. limbatus eggs on A. saligna seeds was also recorded.

Data analysis

The infestation rate, i.e., the percentage of seeds with S. limbatus emergence holes, as well as the percentage of A. saligna seeds with S. limbatus eggs were compared between sites or host species by Fisher exact test. The seed infestation rates were preliminary tested for data overdispersion by analyzing the χ2 approximation of the residual variance (Venables and Ripley 2002; Zuur et al. 2009). Since overdispersion of data was found, overdispersion parameters were included in the corrected models using a quasi-binomial distribution followed by type II ANOVA to test for significance of main effects (Zuur et al. 2009). The seed infestation rate was the response variable, whereas “sampling area” and “year” were the fixed effects in 2019 and 2020, respectively. Corrected analyses were conducted using R software version 4.1.0 (R Development Core Team 2021) at the significance level of 0.05.

Results

Literature search analysis

The literature search on S. limbatus host plant species retrieved about 150 references. After a careful nomenclatural revision, the host range of S. limbatus, as so far described in literature, includes 37 plant genera belonging to three of the six subfamilies in the family Fabaceae:

  1. subfamily Caesalpinioideae: Acacia (16 species), Acaciella (2), Albizia (10), Caesalpinia (1), Calliandra (4), Cassia (4), Cercidium (4), Chloroleucon (2), Delonix (1), Desmanthus (1), Ebenopsis (2), Enterolobium (2), Havardia (4), Hesperalbizia (1), Leucaena (3), Lysiloma (4), Mariosousa (4), Mimosa (1), Neptunia (1), Painteria (1), Parkinsonia (3), Piptadenia (2), Pithecellobium (5), Prosopis (5), Pseudopiptadenia (1), Pseudosamanea (1), Senegalia (15), Sphinga (1), Vachellia (2), Wallaceodendron (1), and Zapoteca (1);
  2. subfamily Cercidoideae: Bauhinia (1);
  3. subfamily Papilionoideae: Arachis (1), Butea (1), Erythrina (1), Glycine (1), and Sesbania (1).

Most host species belong to the subfamily Caesalpinioideae (105), 96 of which to the clade mimosoid, followed by Papilionoideae (5) and a single species of Cercidoideae. The list also comprises the following eight species included as non-host, experimental hosts and uncertain reports: Calliandra humilis Benth., Cercidium texanum A.Gray, Delonix regia (Bojer ex Hook.) Raf., Prosopis juliflora (Sw.) DC., Prosopis velutina Wooton, Senegalia ataxacantha (DC.) Kyal. & Boatwr (syn. A. ataxacantha DC.), Vachellia constricta (Benth.) Seigler & Ebinger, and Vachellia farnesiana (L.) Wight & Arn. (Bridwell 1920; Johnson 1981b; Fox et al. 1996, 2006; Kingsolver 2004; Rink 2013). The comprehensive host range of S. limbatus is provided with up-to-date nomenclature of host species on Table 1.

Table 1.

Updated global host range of Stator limbatus following a literature search analysis and review of valid plant names.

Host species Country (Locality)
Host plant valid name † Original name in the Reference References
Subfamily Caesalpinioideae
Acacia baileyana F.Muell. Acacia baileyana F. Mueller Johnson and Kingsolver 1976 USA (California)
Acacia confusa Merr. Acacia confusa Swezey 1928; Zacher 1952 USA (Hawaii)
Acacia cultriformis A.Cunn. ex G.Don Acacia cultriformis A.Cunn. ex G.Don Johnson and Kingsolver 1976
Acacia cyclops A.Cunn. ex G.Don Acacia cyclops Rink 2013 South Africa (Yzerfontein)
Acacia goldmanii (Britton & Rose) Wiggins Acacia goldmanii (Br. & Rose) Wiggins Johnson 1979 Mexico
Acacia koa A.Gray Acacia koa Swezey 1924 USA (Hawaii)
Acacia koa Gray Stein 1983 USA (Hawaii)
Acacia leptoclada Benth. Acacia leptoclada Romero Gomez et al. 2009
Acacia mangium Willd. Acacia mangium Willd. Pereira et al. 2004; Medina and Pinzón-Florián 2011; Mojena et al. 2018 Brazil (Mato Grosso, Roraima), Colombia
Acacia mearnsii De Wild. Acacia mearnsii De Wild. Oliveira and Costa 2009; Cocco et al. (present paper) Brazil (Rio Grande do Sul), France, Italy
Acacia mearnsii Fox et al. 2006; Rink 2013 South Africa (Tokai, Western Cape)
Acacia melanoxylon R.Br. Acacia melanoxylon R.Br. Johnson and Kingsolver 1976
Acacia pycnantha Benth. Acacia pycnantha Benth. Cocco et al. (present paper) Italy
Acacia podalyriifolia A.Cunn. ex G.Don Acacia podalyriifolia A. Cunningham ex G.Don. Garlet et al. 2011 Brazil (Rio Grande do Sul)
Acacia retinodes Schltdl. Acacia retinodes Schlect. Johnson and Kingsolver 1976 USA (California)
Acacia retusa (Jacq.) R.A.Howard Acacia retusa (Jacq.) R.A.Howard Johnson and Kingsolver 1976 Costa Rica
Acacia richii A.Gray Acacia richei (sic) (richii) Kingsolver 2004
Acacia saligna (Labill.) H.L.Wendl. Acacia saligna (Labill.) H.L.Wendl. Cocco et al. (present paper) Italy, France
Acacia sp. Acacia sp. Johnson 1984; Boroumand 2010; Ghahari and Borowiec 2017 Guatemala, Iran (Bushehr), Mexico
Acaciella angustissima (Mill.) Britton & Rose Acacia angustissima (Mill.) Kuntze Johnson and Kingsolver 1976; Johnson 1984, 1995 Colombia, Mexico, USA (Arizona, Texas), Venezuela
Acacia angustissima Morse and Farrell 2005a Mexico, USA (Texas)
Acacia angustissima angustissima Kingsolver 2004
Acaciella goldmanii Britton & Rose Acacia macmurphyi Wiggins Hetz and Johnson 1988 Mexico
Albizia adinocephala (Donn.Sm.) Britton & Rose ex Record Albizzia (sic) (Albizia) adinocephala Janzen 1980 Costa Rica
Albizia berteriana (DC.) Fawc. & Rendle Pithecellobium fragrans Romero Gomez et al. 2009
Albizia berteroana (Balb. ex DC.) M.Gómez Albizia berteroana Romero Gomez et al. 2009
Albizia caribaea (Urb.) Britton & Rose Albizia caribaea (Urban) Britton & Rose Johnson 1984 Honduras
Albizzia (sic) (Albizia) caribaea Janzen 1980 Costa Rica
Albizia caribaea Romero Gomez et al. 2009
Albizia niopoides var. niopoides Romero Gomez et al. 2009
Albizia chinensis (Osbeck) Merr. Albizzia (sic) (Albizia) chinensis Zacher 1952
Albizia julibrissin Durazz. Albizia julibrissin Fox et al. 2006
Albizia lebbeck (L.) Benth. Albizia lebbeck Benth. Lugo-García et al. 2015 Mexico
Albizia lebbek (sic) lebbeck (L.) Benth. Hetz and Johnson 1988; Johnson 1995 Mexico, Venezuela
Albizzia lebbek (sic) (Albizia lebbeck) Bridwell 1920 USA (Hawaii)
Albizzia (sic) (Albizia) lebbeck (L.) Benth. Nascimento 2009 Brazil (Rio de Janeiro)
Albizia saman (Jacq.) Merr. Samanea saman Bridwell 1920; Morse and Farrell 2005a Panama, USA (Hawaii), Venezuela
Pithecolobium (sic) (Pithecellobium) (= Samanea) saman Zacher 1952
Pithecellobium saman (Jacq.) Merrill Johnson 1984 Guatemala
Pithecellobium saman (Jacquin) Bentham Johnson 1995 Ecuador, Venezuela
Pithecellobium saman Janzen 1980 Costa Rica
Samanea saman (Jacq.) Merrill Johnson and Kingsolver 1976 Costa Rica
Albizia saponaria Blume ex Miq. Albizia saponaria Kingsolver 2004
Albizia sinaloensis Britton & Rose Albizia sinaloensis Britt. & Rose Hetz and Johnson 1988; Johnson 1995 Mexico
Albizia sp. Albizia sp. Johnson 1984, 1995 Brazil (Rio de Janeiro), Ecuador, Honduras, Venezuela
Caesalpinia pulcherrima (L.) Sw. Caesalpinia pulcherrima Fox et al. 2006
Calliandra calothyrsus Meisn. Calliandra calothyrsus Meissn. Johnson and Lewis 1993 Nicaragua
Calliandra eriophylla Benth. Calliandra eriophylla Bentham Johnson 1979 USA (Arizona)
Calliandra houstoniana (Mill.) Standl. Johnson 1984 Mexico, Guatemala
Calliandra houstoniana var. calothyrsus (Meissn.) Barneby Calliandra confusa Sprague & Riley Johnson 1984 Panama
Calliandra humilis Benth. ‡ Calliandra humilis Johnson 1981b
Calliandra humilis humilis Kingsolver 2004
Calliandra humilis var. reticulata (A.Gray) L.D.Benson Calliandra humilis reticulata Kingsolver 2004
Calliandra sp. Calliandra sp. Johnson and Kingsolver 1976; Johnson 1984; Morse and Farrell 2005a Costa Rica, Mexico, Venezuela
Cassia fistula L. Cassia fistula Kingsolver 2004
Cassia grandis L.f. Cassia grandis Kingsolver 2004
Cassia javanica L. Cassia javanica javanica Kingsolver 2004
Cassia javanica subsp. nodosa (Buch.-Ham. ex Roxb.) K.Larsen & S.S.Larsen Cassia javanica indochinensis Kingsolver 2004
Cassia moschata Kunth *
Cassia leiandra Benth. *
Cassia moschata Morse and Farrell 2005b
Cercidium floridum Torr. Cercidium floridum subsp. floridum Romero Gomez et al. 2009
Parkinsonia florida Kingsolver 2004; Fox et al. 2006
Cercidium torreyanum Zacher 1952
Cercidium floridum Bentham Johnson and Kingsolver 1976 USA (Arizona, California)
Cercidium floridum (Benth.) Fox et al. 1996, 2001; Stillwell and Fox 2005 USA (California)
Cercidium macrum I.M.Johnst. Parkinsonia texana var. macra Romero Gomez et al. 2009
Parkinsonia texana macra Kingsolver 2004
Parkinsonia macra (Johnst.) Fox et al. 1996
Parkinsonia macra Nilsson and Johnson 1993 Mexico, USA (Texas)
Cercidium microphyllum Rose & I.M.Johnst. Cercidium microphyllum (Torr.) Rose & Johnst. Johnson and Kingsolver 1976 Mexico, USA (Arizona)
Cercidium microphyllum (Benth.) Fox et al. 2001 USA (California)
Cercidium microphyllum Morse and Farrell 2005a USA (Arizona)
Parkinsonia microphylla Stillwell and Fox 2005
Cercidium texanum A.Gray ‡ Parkinsonia texana texana Kingsolver 2004
Parkinsonia texana (A.Gray) S.Watson ‡ Fox et al. 1996 USA (Texas)
Cercidium sp. Cercidium sp. Johnson 1984 Mexico
Chloroleucon mangense (Jacq.) Britton & Rose Chloroleucon mangense Morse and Farrell 2005b
Chloroleucon mangense (Jacquin) Macbride Johnson 1995 Venezuela
Chloroleucon tenuiflorum (Benth.) Barneby & J.W.Grimes Pithecellobium scalare Griseb. Johnson 1984 Brazil (Rio de Janeiro)
Delonix regia (Bojer ex Hook.) Raf. § Delonix regia § Kingsolver 2004
Desmanthus bicornutus S.Watson Desmanthus bicornutus Kingsolver 2004
Ebenopsis confinis (Standl.) Britton & Rose Ebenopsis confinis Romero Gomez et al. 2009
Ebenopsis ebano (Berland.) Barneby & J.W.Grimes Ebenopsis ebano Romero Gomez et al. 2009
Chloroleucon ebano Nilsson and Johnson 1993 USA (Arizona)
Pithecellobium ebano Kingsolver 2004
Siderocarpus flexicaule (sic) (Siderocarpos flexicaulis) Cushman 1911 USA (Texas)
Ebenopsis sp. Siderocarpus (sic) (Siderocarpos) sp. Zacher 1952; Romero Gomez et al. 2009
Enterolobium contortisiliquum (Vell.) Morong Enterolobium contortisiliquum (Vell.) Morong Meiado et al. 2013 Brazil (Pernambuco)
Enterolobium timbouva Mart. Enterolobium timbouva Mart. Meiado et al. 2013 Brazil (Pernambuco)
Havardia acatlensis (Benth.) Britton & Rose Havardia acatlensis Romero Gomez et al. 2009
Havardia mexicana (Rose) Britton & Rose Havardia mexicana Romero Gomez et al. 2009
Pithecolobium (sic) (Pithecellobium) mexicanum F. N. Rose Johnson and Kingsolver 1976
Havardia pallens (Benth.) Britton & Rose Pithecellobium pallens (Bentham) Standl. Johnson and Kingsolver 1976 USA (Texas)
Havardia pallens Morse and Farrell 2005a Mexico
Pithecolobium (sic) (Pithecellobium) brevifolium Bentham Johnson and Kingsolver 1976
Havardia sonorae (S.Watson) Britton & Rose Havardia sonorae Romero Gomez et al. 2009
Pithecellobium sonorae S. Wats. Johnson and Kingsolver 1976 Mexico
Hesperalbizia occidentalis (Brandegee) Barneby & J.W.Grime Albizia plurijuga Romero Gomez et al. 2009 Mexico
Albizia occidentalis Brandegee Hetz and Johnson 1988
Leucaena diversifolia (Schltdl.) Benth. Leucaena diversifolia Romero Gomez et al. 2009
Acacia diversifolia Romero Gomez et al. 2009
Leucaena leucocephala (Lam.) de Wit Leucaena leucocephala (Lam.) de Wit. Johnson 1984 Mexico
Leucaena leucocephala subsp. glabrata (Rose) Zárate Leucaena leucocephala subsp. glabrata Romero Gomez et al. 2009
Leucaena pulverulenta (Schltdl.) Benth. Leucaena pulverulenta (Schl.) Bentham Johnson and Kingsolver 1976 USA (Texas)
Leucaena trichandra (Zucc.) Urb. Leucaena diversifolia subsp. stenocarpa Romero Gomez et al. 2009
Leucaena guatemalensis Britt. & Rose Johnson 1979 Mexico
Leucaena guatemalensis (Britt. & Rose) Hetz and Johnson 1988 Mexico
Lysiloma acapulcense (Kunth) Benth. Lysiloma acapulcense Romero Gomez et al. 2009 Mexico
Lysiloma acapulcensis (sic) (acapulcense) Bentham Hetz and Johnson 1988 Honduras
Lysiloma acapulcensis (sic) (acapulcense) Kunth. Benth. Johnson 1984 Guatemala
Lysiloma divaricatum (Jacq.) J.F.Macbr. Lysiloma divaricata (Jacq.) MacBride Johnson and Kingsolver 1976; Johnson 1984 Mexico
Lysiloma divaricada (sic) (divaricata) de Lorea Barocio et al. 2006
Lysiloma divaricatum Romero Gomez et al. 2009
Lysiloma microphyllum Romero Gomez et al. 2009
Lysiloma latisiliquum (L.) Benth. Lysiloma latisiliquum (L.) Benth. Johnson 1984 Mexico
Lysiloma tergeminum Benth. Lysiloma tergeminum Romero Gomez et al. 2009
Lysiloma watsonii Rose Lysiloma watsonii Romero Gomez et al. 2009
Lysiloma thornberi Britt. & Rose Johnson 1979 USA (Arizona)
Lysiloma thornberi Zacher 1952
Lysiloma microphylla thornberi Kingsolver 2004
Lysiloma microphyllum var. thornberi Romero Gomez et al. 2009
Lysiloma sp. Lysiloma sp. Johnson and Kingsolver 1976; Johnson 1984 Costa Rica; Mexico
Mariosousa acatlensis (Benth.) Seigler & Ebinger Acacia acatlensis Bentham Johnson and Kingsolver 1976 Mexico
Mariosousa coulteri (Benth.) Seigler & Ebinger Acacia coulteri Bentham Johnson and Kingsolver 1976 Mexico
Acacia coulteri Romero Gomez et al. 2009
Mariosousa coulteri Lugo-García et al. 2015
Acacia near coulteri Bentham Johnson and Kingsolver 1976 Mexico
Mariosousa heterophylla (Benth.) Seigler & Ebinger Acacia willardiana Rose Johnson and Kingsolver 1976 Mexico
Mariosousa millefolia (S.Watson) Seigler & Ebinger Acacia millefolia Wats. Johnson and Kingsolver 1976 USA (Arizona)
Mimosa distachya var. laxiflora (Benth.) Barneby Mimosa laxiflora Benth. Lugo-García et al. 2015 Mexico
Mimosa sp. Mimosa sp. de Lorea Barocio et al. 2006; Romero Gomez et al. 2009 Mexico
Neptunia plena (L.) Benth. Neptunia plena Kingsolver 2004
Painteria leptophylla (DC.) Britton & Rose Painteria leptophylla (DC.) Britton & Rose de Jesús Parra-Gil et al. 2020 Mexico
Parkinsonia aculeata L. Parkinsonia aculeata Linnaeus Johnson and Kingsolver 1976 Mexico, USA (Arizona, Texas)
Parkinsonia aculeata Morse and Farrell 2005a USA (Texas)
Acacia aculeata Zacher 1952
Parkinsonia florida subsp. peninsulare (Rose) J.E.Hawkins & Felger Cercidium floridum subsp. peninsulare Romero Gomez et al. 2009
Parkinsonia praecox (Ruiz & Pav.) Hawkins Parkinsonia praecox Romero Gomez et al. 2009
Cercidium praecox (Ruiz & Pav.) Harms Johnson and Kingsolver 1976 Mexico
Piptadenia flava (Spreng. ex DC.) Benth. Piptadenia flava Janzen 1980 Costa Rica
Parkinsonia flava Romero Gomez et al. 2009
Piptadenia obliqua (Pers.) J.F.Macbr. Piptadenia obliqua (Persoon) Macbride Johnson 1995 Venezuela
Piptadenia oblique Morse and Farrell 2005a Venezuela
Pithecellobium candidum (Kunth) Benth. Pithecellobium candidum Bentham Johnson 1995 Ecuador
Pithecellobium dulce (Roxb.) Benth. Pithecellobium dulce (Roxb.) Bentham Johnson and Kingsolver 1976; Johnson 1984, 1995 Colombia, Costa Rica, Ecuador, El Salvador, Guatemala, Honduras, Mexico, Venezuela
Pithecellobium dulce Morse and Farrell 2005a; de Lorea Barocio et al. 2006 Mexico, Ecuador, Venezuela
Pithecolobium (sic) (Pithecellobium) dulce Bridwell 1920; Zacher 1952 USA (Hawaii)
Pithecellobium excelsum (Kunth) Mart. Pithecellobium excelsum Bentham Johnson 1995 Ecuador
Pithecellobium excelsum Morse and Farrell 2005a Ecuador
Pithecellobium oblongum Benth. Pithecellobium oblongum Janzen 1980 Costa Rica
Pithecellobium unguis-cati (L.) Benth. Pithecellobium unguis-cati Morse and Farrell 2005a Venezuela
Pithecolobium unguiscatae (sic) (Pithecellobium unguis-cati) Bridwell 1920 USA (California)
Pithecellobium sp. Pithecellobium sp. Johnson and Kingsolver 1976 El Salvador
Pithecolobium (sic) (Pithecellobium) sp. Bridwell 1920 USA (Hawaii)
Prosopis chilensis (Molina) Stuntz Prosopis chilensis Romero Gomez et al. 2009
Prosopis chilensis (= juliflora) Zacher 1952
Prosopis farcta (Banks & Sol.) J.F.Macbr. Prosopis farcta Boroumand 2010 Iran (Bushehr and Yazd)
Prosopis farcta (Banks & Soland.) Macbr. Shamszadeh et al. 2017 Iran (Yazd)
Prosopis glandulosa var glandulosa Torr. Prosopis glandulosa glandulosa Kingsolver 2004
Prosopis glandulosa var. torreyana (L.D.Benson) M.C.Johnst. Prosopis glandulosa torreyana Kingsolver 2004
Prosopis juliflora (Sw.) DC. ‡ Prosopis juliflora Bridwell 1920; Kingsolver 2004; Fox et al. 2006
Prosopis velutina Wooton ‡ Prosopis velutina Johnson 1981b
Pseudopiptadenia inaequalis (Benth.) Rauschert Piptadenia inaequalis Bentham Johnson 1995 Venezuela
Piptadenia inaequalis Morse and Farrell 2005a Venezuela
Pseudosamanea guachapele (Kunth) Harms Pseudosamanea guachapele Amarillo‐Suárez et al. 2011
Albizia guachepele (sic) (guachapele) (HBK.) Dugand Johnson 1995 Colombia
Senegalia ataxacantha (DC.) Kyal. & Boatwr ‡ Acacia ataxacantha Rink 2013 South Africa
Senegalia berlandieri (Benth.) Britton & Rose Acacia berlandieri Bentham Johnson and Kingsolver 1976 Mexico, USA (Texas)
Acacia berlandieri Amarillo‐Suárez et al. 2011 USA (Texas)
Senegalia gaumeri (S.F.Blake) Britton & Rose Acacia gaumeri Blake Johnson 1984 Honduras, Mexico
Acacia gaumeri Morse and Farrell 2005a Mexico
Senegalia gilliesii (Steud.) Seigler & Ebinger Acacia furcatispina Romero Gomez et al. 2009
Senegalia glomerosa (Benth.) Britton & Rose Acacia glomerosa Romero Gomez et al. 2009
Acacia near glomerosa Bentham Johnson and Kingsolver 1976 Mexico
Senegalia greggii (A.Gray) Britton & Rose Acacia greggii A. Gray Johnson and Kingsolver 1976 Mexico, USA (Arizona, California, Texas)
Acacia greggii Morse and Farrell 2005a; Amarillo‐Suárez et al. 2011 USA (Arizona)
Senegalia hayesii (Benth.) Britton & Rose Acacia hayesii Romero Gomez et al. 2009
Senegalia occidentalis (Rose) Britton & Rose Acacia occidentalis Rose Johnson and Kingsolver 1976 Mexico
Senegalia picachensis (Brandegee) Britton & Rose Acacia picachensis T. S. Brandg. Johnson 1984 Mexico
Senegalia polyphylla (DC.) Britton & Rose Acacia polyphylla DC. Johnson 1995; Johnson and Siemens 1995 Colombia, Venezuela
Senegalia riparia (Kunth) Britton & Rose Acacia riparia Romero Gomez et al. 2009
Senegalia roemeriana (Scheele) Britton & Rose Acacia roemeriana Scheele Johnson and Kingsolver 1976 USA (Texas)
Senegalia tamarindifolia (L.) Britton & Rose Acacia tamarindifolia (L.) Willdenow Johnson 1995; Johnson and Siemens 1995 Venezuela
Acacia tamarindifolia Morse and Farrell 2005a Martinique
Senegalia tenuifolia (L.) Britton & Rose Acacia tenuifolia (L.) Willd. Johnson and Kingsolver 1976; Johnson 1984 Costa Rica, Mexico
Senegalia wrightii (Benth.) Britton & Rose Acacia wrightii Bentham Johnson and Kingsolver 1976 USA (Texas)
Acacia wrightii Morse and Farrell 2005a Mexico, USA (Texas)
Sphinga platyloba (DC.) Barneby & J.W.Grimes Sphinga platyloba Morse and Farrell 2005b
Pithecellobium platyloba (sic) (platylobum) Janzen 1980 Costa Rica
Havardia platyloba Romero Gomez et al. 2009
Vachellia constricta (Benth.) Seigler & Ebinger ‡ Acacia constricta Johnson 1981b
Vachellia farnesiana (L.) Wight & Arn. ‡ Acacia farnesiana Bridwell 1920
Acacia farnesiana Zacher 1952
Wallaceodendron celebicum Koord. Wallaceodendron celebicum Bryan 1932 USA (Hawaii)
Zapoteca portoricensis (Jacq.) H.M.Hern. Zapoteca portoricensis Morse and Farrell 2005b
Subfamily Cercidoideae
Bauhinia purpurea L. Bauhinia purpurea L. Fox et al. 2006
Subfamily Papilionoideae
Arachis hypogaea L. Arachis hypogaea Kingsolver 2004
Butea monosperma (Lam.) Kunze Butea monosperma Romero Gomez et al. 2009
Erythrina monosperma Zacher 1952
Erythrina sandwicensis O.Deg. Erythrina sandwicensis Kingsolver 2004
Glycine max (L.) Merr. Glycine max Kingsolver 2004
Sesbania sp. Sesbania sp. Romero Gomez et al. 2009

Seed infestation

The field surveys carried out in 2019–2020 demonstrated the presence of the seed-feeding beetle S. limbatus both in Sardinia (Italy) and Corsica (France) islands on the host plant A. mearnsii (Table 1). In Sardinia, the beetle emerged from seeds collected in all the 14 sites in both the central eastern and southwestern sampling areas. In 2019, the infestation rates ranged from 24.3 to 74.2% and from 39.3 to 83.4% in Berchida-Bidderosa and Monte LinasMarganai areas, respectively, showing significant differences among sampling sites (Fisher tests: χ2 = 1074.85; df = 5; P < 0.001 and χ2 = 404.83; df = 7; P < 0.001, respectively) (Table 1). Overall, the seed infestation rate by S. limbatus did not differ between central eastern and southwestern sampling areas (F = 0.496; df = 1.13; P = 0.494). In 2020, the infestation in the central eastern sampling sites also differed significantly among sites (range = 85.4–90.8%) (Fisher test: χ2 = 31.42; df = 5; P < 0.001), and increased significantly compared to 2019 (F = 16.206; df = 1.11; P = 0.002). A large majority of A. mearnsii seeds (≥ 96.5% of seeds sampled in the various sites) showed S. limbatus eggs (up to 18 eggs in a single seed) and ≥ 98.4% of the infested seeds exhibited a single exit hole (Fig. 3A).

Figure 3.

Acacia seeds (with arils on top) infested by Stator limbatus, with eggs and exit holes A S. limbatus adult emerging from an Acacia mearnsii seed with 11 eggs B S. limbatus adult emerging from A. pycnantha seed with two exit holes C A. saligna seed with a S. limbatus egg and one exit hole.

Acacia pycnantha trees sampled in central eastern Sardinia in both 2019 and 2020 (site 1) showed the highest infestation levels (85.1 and 95.1%, respectively) compared to A. mearnsii sites in the same area (Table 1). Of A. pycnantha infested seeds sampled in 2019 and 2020, 29.5 and 45.2%, respectively, exhibited two exit holes and up to 28 eggs were recorded in a single seed (Fig. 3B). Both the percentage of infested seeds and seeds with two holes increased significantly from 2019 to 2020 (Fisher tests: χ2 = 48.73; df = 1; P < 0.001 and χ2 = 24.03; df = 1; P < 0.001, respectively).

Pods and seeds of A. saligna were collected in the surroundings of infested A. mearnsii and A. pycnantha trees in two and nine sites in central eastern Sardinia (Table 2). The infestation rate was very low in both years and was significantly the highest at the site 5 in both 2019 (4%) (Fisher test: χ2 = 6.32; df = 1; P = 0.033) and 2020 (2.6%) (Fisher test: χ2 = 53.74; df = 8; P < 0.001). However, S. limbatus eggs were recorded on up to 52.8 and 79.6% of A. saligna seeds in 2019 and 2020, respectively (Fig. 3C). A single seed harbored up to six eggs. The seed infestation rate ranged in 2020 from 0 to 2.6% regardless of the distance from infested Acacia spp. trees, whereas A. saligna seeds with the highest percentage of beetle eggs (sites 1, 4, 5, and 6, range 45.1–79.6%) were recorded on trees <5 m apart from infested trees (Table 2).

Table 2.

Locations of sampling sites in Sardinia (Italy) and Corsica (France), and seed infestation rates of Acacia pycnantha and A. mearnsii by Stator limbatus.

Site no. WGS84 Coordinates (°N, °E) Sampling date Host plant Sampled seeds (no.) Infestation rate (%) †
Sardinia, Berchida-Bidderosa area, 2019
1 40.451995, 9.778190 18/09/2019 A. pycnantha 315 85.1 a
2 40.459980, 9.785646 18/09/2019 A. mearnsii 199 38.7 d
3 40.457190, 9.793082 18/09/2019, 01/10/2019 A. mearnsii 3459 74.2 b
4 40.463992, 9.798704 18/09/2019, 01/10/2019 A. mearnsii 1030 49.3 d
5 40.545390, 9.782090 18/09/2019 A. mearnsii 61 45.9 d
6 40.549220, 9.788000 18/09/2019, 01/10/2019 A. mearnsii 1137 24.3 e
7 40.578073, 9.777057 18/09/2019, 01/10/2019 A. mearnsii 3639 67.5 c
Sardinia, Berchida-Bidderosa area, 2020
1 40.451995, 9.778190 10/08/2020 A. pycnantha 2415 95.1 a
2 40.459980, 9.785646 10/08/2020 A. mearnsii 1784 90.8 b
3 40.457190, 9.793082 10/08/2020 A. mearnsii 2234 89.0 bc
4 40.463992, 9.798704 10/08/2020 A. mearnsii 1704 86.5 d
5 40.545390, 9.782090 10/08/2020 A. mearnsii 1023 85.4 d
6 40.578073, 9.777057 10/08/2020 A. mearnsii 390 87.2 cd
7 40.549220, 9.788000 10/08/2020 A. mearnsii 1574 89.8 bc
Sardinia, Monte Linas – Marganai area, 2019
10 39.421480, 8.716520 23/09/2019 A. mearnsii 226 61.9 cde
11 39.398540, 8.695790 23/09/2019 A. mearnsii 199 54.3 e
12 39.391094, 8.675427 23/09/2019 A. mearnsii 341 65.4 cd
13 39.396532, 8.658998 23/09/2019 A. mearnsii 671 66.6 c
14 39.393961, 8.663604 23/09/2019 A. mearnsii 980 59.8 de
15 39.391863, 8.669016 23/09/2019 A. mearnsii 951 79.4 b
16 39.420067, 8.713574 23/09/2019 A. mearnsii 1187 83.4 a
17 39.449340, 8.733530 23/09/2019 A. mearnsii 428 39.3 f
Corsica, 2019
18 42.546699, 9.525582 29/10/2019 A. mearnsii - n.a.
19 42.125300, 9.510656 07/11/2019 A. mearnsii - n.a.
Corsica, 2020
18 42.546576, 9.5246522 20/08/2020 A. mearnsii - n.a.
19 42.125065, 9.510606 20/08/2020 A. mearnsii 8500 56.0
21 41.380217, 9.222299 03/09/2020 A. mearnsii - n.a.

In Corsica, S. limbatus adults were recorded in all four sampling sites. In 2019, adults emerged in both eastern (site 19) and northeastern (site 18) sites from A. mearnsii seeds. Most seeds exhibited exit holes and egg chorions of S. limbatus, although a few individuals were recorded: four adults from site 19 and one from site 18. In 2020, S. limbatus adults were further recovered in sites 18 and 21, in which more than 400 adults emerged from samples of A. mearnsii seeds of unknown sizes. In site 19, the infestation level by S. limbatus was 56.0%. Seeds of A. saligna were collected in site 20, where the infestation rate was 0.2%.

Table 3.

Locations of sampling sites in Sardinia (Italy) and Corsica (France), and seed infestation rates of Acacia saligna seeds by Stator limbatus.

Site no. WGS84 Coordinates (°N, °E) Sampling date Distance from infested Acacia trees Sampled seeds (no.) Infestation rate (%) † Seeds with S. limbatus eggs (%) †
Sardinia, Berchida-Bidderosa area, 2019
4 40.463799, 9.799295 18/09/2019 < 5 m 156 0 b 44.9 a
5 40.545420, 9.782050 18/09/2019 < 5 m 75 4.0 a 52.8 a
Sardinia, Berchida-Bidderosa area, 2020
1 40.451980, 9.778390 10/08/2020 < 5 m 1550 0 d 57.2 b
4 40.463799, 9.799295 10/08/2020 < 5 m 524 0.6 abc 60.7 b
5 40.545420, 9.782050 10/08/2020 < 5 m 116 2.6 a 79.6 a
40.546396, 9.782224 10/08/2020 < 100 m 864 0.3 bcd 24.4 d
40.546109, 9.781190 10/08/2020 < 100 m 867 0 d 18.0 e
6 40.549240, 9.788131 10/08/2020 < 5 m 859 0 d 45.1 c
40.549022, 9.786670 10/08/2020 < 100 m 1237 0.2 bcd 22.5 d
8 40.618420, 9.743740 10/08/2020 > 100 m 981 0 d 3.0 g
9 40.592818, 9.710812 17/08/2020 > 100 m 596 0.2 bcd 8.9 f
Corsica, 2020
20 41.380217, 9.222299 27/08/2020 - 4360 0.2 n.a.

Discussion

The extensive collection of S. limbatus during the field surveys in 2019 and 2020 in Sardinia and Corsica following the first record in 2018 indicates that the seed beetle has found suitable climatic conditions and has established in Europe. Stator limbatus can be considered established according to the definition of Yus-Ramos et al. (2014), i.e., a species able to reproduce successfully in natural ecosystems. Stator limbatus exhibits biological features that could support its further spread in Europe. At first, this species has a wide host range worldwide, with about 15 species reported in Europe (Euro+Med 2021; GBIF 2021). Furthermore, its native geographic range includes diverse climates, spanning from dry forests of northern South America to deserts of Central America and southwestern United States (Stillwell and Fox 2009). In addition, this bruchid developed under laboratory conditions also on non-native species, including Acacia cyclops A.Cunn. G.Don and S. ataxacantha (syn. A. ataxacantha) (native to Australia and South Africa, respectively) (Rink 2013), as well as non-host species, such as C. humilis, C. texanum, P. juliflora, P. velutina, V. constricta, and V. farnesiana (Bridwell 1920; Johnson 1981b; Fox et al. 1996). Finally, S. limbatus have shown adaptive oviposition phenotypic plasticity in response to host species, as fewer and bigger eggs are laid on exotic or unfavorable hosts (Amarillo-Suarez et al. 2017). Such maternal egg-size plasticity is suggested to be an ancestral trait influencing the evolution of the diet breadth (Amarillo-Suárez and Fox 2006). Overall, the wide presence of host species of S. limbatus in Europe, its strong host shift potential, and climate adaptation suggest its possible spread in Mediterranean environments, and its presence in unsampled areas cannot be ruled out.

This species was recovered from Acacia spp. seeds in Sardinia, in multiple sites distant up to 150 km, and Corsica, in four areas distant about 130 km. Even though the country of first introduction in Europe remains undetermined, the wide presence of this alien insect in distant areas supports the hypothesis that its introduction occurred several years ago. The introduction of S. limbatus in Europe was most likely accidental and its detection unexpected. The pathway of first introduction is presently unknown, as no specific custom interception has so far been reported. With regard to pathways of secondary spread, in view of its wide host range and endophytic behavior of larvae, we may assume that it was introduced through movement of contaminated commodities, i.e., plants for planting, as a parasite of seeds (CBD 2014; Faulkner et al. 2020). In fact, after its first introduction, a secondary spread pathway may have occurred as a result of movement of contaminated plants (with pods) or seeds of A. saligna, A. mearnsii, and A. pycnantha, which are commonly planted in southern Europe and significantly traded. In addition, the very large number of different host species should be taken into account (Table 1), as many are common ornamental, i.e., Albizia spp., Leucaena spp., Parkinsonia spp., and Glycine max (L.) Merr., or forestry and multipurpose species, i.e., Acacia spp., in the Mediterranean area. Therefore, in order to investigate the S. limbatus presence or intercept its introduction in areas nearby Sardinia and Corsica, specific monitoring plans on its host species should be set up in southern France and mainland Italy. Although the pathways of first introduction and secondary spread are generally not known for bruchid seed beetles, several authors suggest introductions through importation of seed or nursery stocks of host plant species for ornamental or forestry purposes, e.g., Bruchidius terrenus (Sharp, 1886) on Albizia julibrissin Durazz. and Amblycerus robiniae (Fabricius, 1781) on Gleditsia triacanthos L. in the United States (Kingsolver 2004; Hoebeke et al. 2009; Yus-Ramos et al. 2014).

The introduction of alien seed beetles in Europe shows an increasing trend in the last 20 years, in accordance with the worldwide trend described by Seebens et al. (2017). Beenen and Roques (2010) reported 14 Bruchinae alien species in Europe, seven of which introduced before 1900, three species in the period 1901–1950, two in 1951–2000, and finally two species reported from 2001 to 2010. Yus-Ramos et al. (2014) further extended the list of alien bruchids in Europe to a total of 42 species, including four recent introductions, namely Bruchidius radiannae Anton & Delobel, 2003 and Caryedon acaciae (Gyllenhal, 1833) on Vachellia karroo (Hayne) Banfi & Galasso (syn. Acacia karroo Hayne) in 2007 in Spain (Yus Ramos and Coello García 2007, 2008), Acanthoscelides macrophthalmus (Schaeffer, 1907) on Leucaena leucocephala (Lam.) de Wit in Cyprus in 2007 (Vassiliou and Papadoulis 2008), and B. terrenus on A. julibrissin in Bulgaria in 2009 (Stojanova 2010). Furthermore, A. robiniae was reported on G. triacanthos in Romania in 2018 following an unconfirmed report in Hungary in 1986 (Rădac et al. 2021). Therefore, according to literature reports, seven species of bruchids have been reported in Europe in the last 20 years. In both Corsica and Sardinia, S. limbatus larvae developed on seeds of A. mearnsii, a tree native to Australia which has shown to be invasive in Europe, South America, and Africa. This insect-host association has been previously reported in Brazil, where an infestation rate of 44.3% was observed (Oliveira and Costa 2009), and South Africa (Rink 2013). Acacia mearnsii is cultivated in Brazil for tannins, cellulose, and charcoal production (Garlet et al. 2011), whereas in Europe and in South Africa, presently, this species has a lower significant economic importance and is rather invasive (Souza-Alonso et al. 2017; Railoun et al. 2021).

In Sardinia, beetle adults emerged abundantly also from A. pycnantha seeds, and, interestingly, 45% of sampled seeds showed two exit holes, differently from A. mearnsii seeds which showed a single exit hole. This brings evidence that A. pycnantha seeds support the development of more than one larva of S. limbatus, most likely because of the bigger size of its seeds compared to those of A. mearnsii. In central eastern Sardinia, the infestation rate was more homogeneous among sampling sites in 2020 than in 2019, as the range decreased from 49.9% (24.3–74.2%) in 2019 to 5.4% (85.4–90.8%) in 2020. Moreover, infestation rates increased significantly on both A. mearnsii and A. pycnantha. However, the seed production of trees in the sampling sites was not quantitatively estimated being beyond the aims of the study. Estimates of seed infestation rates with no assessment of tree seed production and over such a short period, i.e. two years, prevent to infer on spatio-temporal population trends of S. limbatus. The same insect abundance can, in fact, cause high infestation rates in the event of low seed production or low rates when seed production is high. Nonetheless, although Acacia spp. seed production and accumulation may vary widely, Australian and African species usually produce large or very large quantities of seed and may have large soil-stored seed banks (Gibson et al. 2011). High production of seeds for the three investigated species has been observed both in the native and in the invaded ranges, e.g., A. mearnsii in South Africa (Impson et al. 2021), being one of the drivers of invasiveness at the global level. Indeed, large amounts of pods were observed on Acacia spp. trees as well as seeds in the topsoil in both 2019 and 2020 (A. Cocco, Y. Petit, pers. obs.). Furthermore, high numbers of seedlings were observed in the sampling sites with A. mearnsii.

Previous studies on infestation by S. limbatus on Fabaceae species reported seed damages of 15% on E. timbouva (Meiado et al. 2013), 19% on Acacia mangium Willd. (Mojena et al. 2018), and 70% on Acacia podalyriifolia A.Cunn. ex G.Don (Garlet et al. 2011) in Brazil. In Mexico, seed infestation rates of 16.8% were observed on Painteria leptophylla (DC.) Britton & Rose (de Jesús Parra-Gil et al. 2020) and 33.6% on Mariosousa coulteri (Benth.) Seigler & Ebinger by both S. limbatus and Merobruchus santarosae Kingsolver, 1989 (Coleoptera, Chrysomelidae) (Romero Gomez et al. 2009). Susceptibility to S. limbatus widely varied among hosts and areas; however, comparisons are difficult, as seed infestation rates are influenced by a number of abiotic and biotic factors, including seed availability and environmental conditions. Despite its recent report in South Africa, S. limbatus has not been reported infesting A. pycnantha seeds (Rink 2013; Magona et al. 2018).

A word of caution is in order with regard to A. saligna as a host species for S. limbatus. In fact, infestation rates were very low in both years and countries, and the highest values (4% in 2019 and 2.6% 2020) were observed in the same site. Nonetheless, infestation by S. limbatus on A. saligna seeds was not limited to a single site, as infested plants were observed in both Sardinia and Corsica. Moreover, beetle eggs were observed on up to 80% of A. saligna seeds, especially on plants near to infested Acacia spp. trees. This could be due to an opportunistic egg-laying behavior on the nearest alternative hosts. Furthermore, oviposition on A. saligna indicates that seeds had no antixenotic effect on female oviposition and oviposition is promoted by suitable hosts nearby. Chemical or physical barriers on A. saligna seeds preventing larval development cannot be ruled out and would require further investigations. Laboratory tests carried out in South Africa investigating the oviposition preference showed that S. limbatus females accepted A. saligna seeds for oviposition, together with seeds of A. cyclops, A. mearnsii, Paraserianthes lophantha (Willd.) I.C.Nielsen (invasive non-native species in South Africa), and Vachellia tortilis (Forssk.) Galasso & Banfi [syn. Acacia tortilis (Forssk.) Hayne], S. ataxacantha, Senegalia caffra (Thunb.) P.J.Hurter & Mabb. [syn. A. caffra (Thunb.) Willd.], Senegalia nigrescens (Oliv.) P.J.Hurter [syn. A. nigrescens (Oliv.)] and Vachellia sieberiana var. woodii (Burtt Davy) Kyal. & Boatwr. [syn. A. sieberiana var. woodii (Burtt Davy) Keay & Brenan] (native species to South Africa). However, adults emerged only from A. mearnsii, A. cyclops, and S. ataxacantha, indicating that food availability may not be the only factor limiting the larval development (Rink 2013).

In view of its high seed infestation rates, S. limbatus has been suggested to play a role as biocontrol agent of invasive non-native Acacia species (Rink 2013). In South Africa, extensive biological control programs have been developed against invasive tree species, as, for example, the release of A. macrophthalmus for biological control of L. leucocephala in 1999 (Olckers 2004). Five seed-weevil Melanterius spp. (Colepotera, Curculionidae) were introduced from Australia in different periods to reduce the invasiveness of P. lophantha and ten Acacia spp., including the three species investigated in the present paper, i.e., A. mearnsii, A. saligna, and A. pycnantha (Impson et al. 2011). Seed damage caused by weevils varied largely among sites and years from 4% to over 90%. Such variability was explained by a specific 4-year study on MelanteriusAcacia relationship and was mostly due to variable seed quality that resulted in low larval and pupal survival rates (Impson and Hoffmann 2019). Overall, seed-feeders are unlikely to effectively reduce the Acacia spp. density as a stand-alone control agent due to the extraordinarily high prolificacy of plants resulting in huge accumulation of long-lived seeds in the soil. In fact, effective results were obtained through the release of the flower-galling midge, Dasineura rubiformis Kolesik (Diptera, Cecidomyiidae) complemented by a seed-feeding weevil, Melanterius maculatus Lea (Coleoptera, Curculionidae), which caused a strong reduction of seed production of A. mearnsii (Impson et al. 2021). This reduction is expected to curb the accumulation rate of the seed banks and, in the medium-long term, reduce the spread of the invasive species. Besides a potential biocontrol agent of invasive plant species, further beneficial environmental effects by S. limbatus may be represented by the promotion of seed germination, e.g., on Enterolobium contortisiliquum (Vell.) Morong and E. timbouva Mart. (Meiado et al. 2013).

The present findings indicate the adaptability of S. limbatus to new host species when established in new areas. Stator limbatus also showed phenotypic plasticity in response to seed size or seed quality (Amarillo-Suárez and Fox 2006), in accordance with findings in other species (Hardy et al. 1992; Tsai et al. 2001). Moreover, this is consistent with results from studies showing that development time decreased and adult mass increased when insects developed on high quality hosts (Lindroth et al. 1991; Stockhoff 1993). Therefore, host shifts on local plants and new host associations cannot be ruled out in Europe in view of its ability to accept and adapt to local hosts. Adaptation to new or non-preferred host species has been observed on other coleopteran alien species, such as the red palm weevil Rhynchophorus ferrugineus (Olivier, 1790) (Coleoptera, Dryophthoridae) on the dwarf palm, Chamaerops humilis L. (Cocco et al. 2019). Importantly, S. limbatus has been reported on > 90 host species and ≥ 20 genera (de Jesús Parra-Gil et al. 2020), which is one of the widest host ranges within the Bruchinae. In view of its tropic spectrum, it has been classified as polyphagous, i.e., feeding in the seeds of various plant genera of different subfamilies (Ribeiro-Costa and Almeida 2012; Yus-Ramos 2018). However, its host use is widely variable and it shows local specialization depending on the diversity of available host species (Morse and Farrell 2005a, 2005b). The establishment of S. limbatus in Europe and new associations with A. pycnantha and A. saligna required a redefinition and update of the bruchid host range to facilitate further research on its potential adaptation and spread in Europe. The exact definition of the host range of S. limbatus is not trivial due to nomenclatural issues within the family Fabaceae which have not been resolved (LPWG 2017). In addition, in a number of cases, the literature reported incorrect or partial names for the host plants. The bibliographic search analysis allowed to extend the global host range of S. limbatus to 111 species, in most part belonging to the mimosoid clade of the subfamily Caesalpinioideae (Fabaceae) (LPWG 2017). Synonym issues were resolved, e.g., Acacia diversifolia and Leucaena diversifolia both mentioned by Romero Gomez et al (2009) and synonymized in Leucaena diversifolia (Schltdl.) Benth, and up-to-date nomenclature provide the current and comprehensive overview of the feeding spectrum of S. limbatus. However, some old or unconfirmed reports would require further investigations, e.g., G. max, Wallaceodendron celebicum Koord., and Arachis hypogaea L. (Brian 1932; Kingsolver 2004). Since no previous records were found in literature, A. pycnantha and A. saligna are included in the present paper for the first time in the host range of S. limbatus.

This report of establishment of S. limbatus in Europe contributes to updating the insect worldwide distribution, which now includes North and Central America (native region), South America, South Africa, the Middle East, and southern Europe. Future research is required on known and potential host species in order to investigate its potential distribution and new host associations with native or non-native plant species (Parry et al. 2013). Studies on suitable climatic conditions for S. limbatus development will further assess the risks of spread in the Mediterranean Basin. Such surveys should include also urban habitats, in which seed feeders are frequently found (Branco et al. 2019).

Acknowledgements

The authors gratefully acknowledge Gianluigi Bacchetta (Biodiversity Conservation Centre, University of Cagliari, Italy) for fruitful discussions and technical support, and Roberto Mannu (University of Sassari) for statistical advice. This study was financially supported, in part, by the Project ALIEM “Action pour Limiter les risques de diffusion des espèces Introduites Envahissantes en Méditerranée” PC IFM 2014–2020 and by RESTART-UNINUORO Project “Azioni per la valorizzazione delle risorse agroforestali della Sardegna centrale/Actions for the valorisation of agroforestry resources in central Sardinia” Regione Autonoma della Sardegna, D.G.R. N. 29/1 del 7 June 2018—fondi FSC 2014–2020. AS, GB, and IF gratefully acknowledge University of Sassari for the financial support through “Fondo di Ateneo per la Ricerca 2020”. The authors have declared that no competing interests exist.

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