APHIS Protocols and History of Specimens

Interceptions of suspected quarantine pests are submitted to APHIS-PPQ identifiers located at designated facilities throughout the United States. Specimens are identified to the lowest level needed to determine whether the shipments involve required quarantine measures. Regulatory officials with APHIS-PPQ do not require quarantine treatments for predatory species such as members of the Anthocoridae, thus almost none of the specimens of these insects in the Miami collection had been identified beyond the family level. Once the regulatory status of an intercepted specimen is resolved, the specimen is placed in a port reference collection and the data associated with it are entered into a national database. One of us (TTD) served in Miami, FL as Plant Protection and Quarantine's specialist in Heteroptera from 2001 to 2010, and in that capacity additionally acquired several specimens of Anthocoridae that had been intercepted at ports other than Miami.

Identification of Specimens

Insects were identified by use of published keys (including as needed examination of genitalia), by examination of descriptions in the primary literature, and by inspection of geographically relevant checklists or catalogs of the Heteroptera. Specimens were generally identified to species, although some specimens within difficult complexes such as Orius Wolff, 1811, and Lyctocoris Hahn, 1835, were identified only to genus. Female specimens in difficult groups could often not be identified other than to genus because examination of the male genitalia is needed for full identification. Specimens of Xylocoris Dufour, 1831, and Orius that could not be identified to species are given subgeneric classifications when possible (Carayon 1972b; Péricart 1972). Label information with most specimens included geographic source and commodity of the shipment from which the specimen had been collected. Each specimen was categorized according to Zoogeographic region from which the intercepted specimen had arrived (Darlington 1957): Neotropical (specimens arriving from South America/Central America/West Indies); Nearctic (Mexico); Ethiopian (Sub-Saharan Africa); Oriental (Asia); and Palearctic (Europe/ Mediterranean).

TABLE 1.

DISTRIBUTION OF THE 127 INTERCEPTED SPECIMENS ACROSS FAMILIES, TRIBES, AND GENERA.

Higher-level classification of the Anthocoridae is not completely settled. Beginning with Carayon (1972a), systematic treatments of the Anthocoridae have not always agreed on whether these insects belong in a single family (Anthocoridae) composed of 3 subfamilies (Anthocorinae, Lasiochilinae, Lyctocorinae), or whether the subfamilies deserve family rank (Cassis & Gross 1995; Schuh & Slater 1995). We follow the treatment of Schuh & Slater (1995), and allocate genera among 3 families (Anthocoridae, Lyctocoridae, Lasiochilidae) and 7 tribes within the family Anthocoridae.

Anthocoridae: Oriini

The Oriini is composed of 16 genera (Carayon 1972a; Péricart 1996) including the widespread Orius with 75–80 described species (Ford 1979; Yasunaga 1997; Jung et al. 2011). Interceptions included 2 genera: Orius; and a single specimen of Caffrocoris brincki Carayon, 1961, known only from South Africa (Carayon 1961; Ford 1979). The interceptions of Orius comprised 56 specimens from 9 identified species distributed among 4 zoogeographic regions (Table 2). Seventeen specimens could be identified only to genus, due either to lack of suitable keys, or because no male specimens (needed for examination of genitalia) were available in the interceptions. Members of this genus are commonly associated with flowers and other produce, and are regular interceptions at ports on cut flowers, ornamental plants, and agricultural produce (Herring 1967). Virtually all intercepted specimens were associated with cut flowers, bouquets, or ornamental plants (Table 2). Orius commonly occurs in flowers and bloom clusters under field conditions (Miliczky & Horton 2011). Cut flowers are known important sources of arthropod interceptions in general (Work et al. 2005; McCullough et al. 2006).

Intercepted specimens of Orius that we were able to identify to species included both Old and New World taxa. Orius niger (Wolff, 1811), O. minutus (Linnaeus, 1758), O. majusculus (Reuter, 1879), and O. vicinus (Ribaut, 1923) are Old World species distributed throughout Europe and parts of Asia (Péricart 1996), and were intercepted on shipments from The Netherlands, Israel, and Turkey (Table 2). A fourth Old World species, O. albidipennis (Reuter, 1884) is found throughout North Africa and Asia (Péricart 1996), and was intercepted on Helianthus arriving from Israel (Table 2). Orius peri Carayon, 1976, apparently has been collected only from South Africa (Hernández & Stonedahl 1999), and was intercepted on a shipment of cut flowers from South Africa (Table 2). Two South American species, O. florentiae Herring, 1966, and O. championi Herring, 1966, were intercepted on shipments from Ecuador and Colombia (Table 2). Orius insidiosus (Say, 1832) was intercepted in shipments from Mexico, Central America, the West Indies, and South America. This species is native to the Nearctic/Neotropical Regions, and is geographically widespread in eastern North America and southwards into Central/South America and the West Indies (Henry 1988; Carpintero 2002).

Species of Orius frequently become established in geographic regions outside of their native ranges (Herring 1967; Yasunaga 2000; Lattin 2007ab; Henry 2008; Lewis & Lattin 2010) following accidental introduction into those regions. Two of the Old World species detected in our interceptions, O. albidipennis and O. niger, are currently established in several geographic regions outside of their respective native ranges (Péricart 1996). Orius vicinus, another Old World species intercepted on shipments from Europe (Table 2), is known to be established in North America, apparently since at least the 1930s (Lewis & Lattin 2010). It is also an established introduction in New Zealand, where it is found feeding on pest arthropods in apple orchards (Larivière & Wearing 1994). Orius insidiosus has become established in Hawaii, although possibly as a consequence of intentional introduction (Lattin 2007b). The European/Asian species, O. minutus, was at one time thought to be an established introduction in North America (Lattin et al. 1989), but has since been removed from the North American faunal list (Lewis & Lattin 2010). North American records of this species are actually mistakes in identifications of the non-indigenous O. vicinus (Lewis & Lattin 2010).

Anthocoridae: Cardiastethini

The Cardiastethini presently includes 16 genera of often uncertain systematic affinities distributed extensively in the Old and New World tropics (Ford 1979; Schuh & Slater 1995; Carpintero 2002; Carpintero & Dellapé 2008). Five genera within the Cardiastethini were identified in interceptions from 3 zoogeographic regions (Tables 1 and 2). Specimens were collected from plants, cut flowers, basketware, and luggage (Table 2). Amphiareus constrictus (Stål, 1860) was intercepted in shipments from the Neotropics (South America/Central America/West Indies) and Asia (Table 2). This species is geographically widespread, particularly in the Old and New World tropics (Herring 1967; Ford 1979; Yamada 2008b), and is established as an introduction in many parts of the world, including on a number of oceanic islands (Hawaii — Lattin 2007b; the Galápagos — Herring 1966, Lattin 2007a; Micronesia — Herring 1967; and the Cook Islands — Walker & Deitz 1979). The species apparently is established in western North America, probably through accidental introduction (Lattin & Lewis 2001; Lattin 2007c). As occurs with other members of the Cardiastethini, species of Amphiareus Distant, 1904, are commonly associated with dead leaf clusters, dead trees, decaying fungi, or stacked logs, where they presumably feed on small soft-bodied arthropods such as Psocoptera and mites (Lattin & Lewis 2001; Yamada & Hirowatari 2003; Henry et al. 2008; Yamada 2008b; Jung & Lee 2011a).

Cardiastethus Fieber, 1860 is a large genus of approximately 45 species distributed extensively in tropical and subtropical regions (Ford 1979; Yamada & Hirowatari 2007a). Members of the genus often occur in association with dead plant tissues and leaf litter, where they feed on psocids or other soft-bodied arthropods (Carayon 1957; Styles 1962; Lattin 1999b); some taxa occur on agricultural plants as predators of pest arthropods (Yamada et al. 2008). Cardiastethus is common in shipments of grain and other food stuffs (Herring 1967). Interceptions included 4 specimens from Central America, the West Indies, and Thailand associated with ornamental plants, cut flowers, or baggage (Table 2). Cardiastethus minutissimus Usinger, 1946 is known from Guam, Micronesia, and the Ogasawara Islands, Japan (Usinger 1946; Herring 1967; Yamada & Hirowatari 2007a), and is established as an introduction in Hawaii (Lattin 2007b). Cardiastethus affinis Poppius, 1909 is known from East Africa and India (Yamada et al. 2008).

Physopleurella Reuter, 1884 is a tropical/subtropical genus of 16 described species almost entirely of Old World origin (Yamada & Ishikawa 2011). Members of this genus may often inhabit dead-leaf habitats. Collection records include dead leaves of palmetto, cane, fan- flower, and banana; dead leaves of evergreen trees; dried leaves of hula skirts; and nests of weaverbirds (Usinger 1946, 1951; Lattin 2005b; Yamada & Hirowatari 2007b; Jung & Lee 2011b). Psocids in these habitats may be preferred prey (Swezey 1905; Lattin 2005b). Interceptions included specimens of 2 species from Guyana, Haiti, and the Philippines (Table 2). Physopleurella mundula (White, 1877) was intercepted at the Miami Airport on flowers and on palmetto leaves in luggage; this species is known to occur in Florida, probably as an introduction (Lattin 2005b). According to Lattin (2005b), P. mundula has also been intercepted at airports in Philadelphia (from Mexico) and New Orleans (from Honduras). Physopleurella flava Carayon, 1956 was intercepted on basketware arriving from the Philippines. The species was described from West Africa and appears to be distributed in tropical Africa, Madagascar, and Southeast Asia (Ford 1979; Yamada & Hirowatari 2007b). Its biology is generally unknown, although specimens have been collected from the nests of weaverbirds (Carayon 1958).

Alofa Herring, 1976, includes only a single species, Alofa sodalis (White, 1878). The species was described from Hawaii, originally as a species of Cardiastethus. Alofa sodalis has been collected in dead leaf habitats, detritus, stored goods, and bird nests, where its primary prey may often be psocids (Usinger 1951; Carayon 1958). The insect is also a predator of pest Lepidoptera on coconut in India (Nasser & Abdurahiman 1990). Alofa sodalis is geographically widespread, described as “cosmopolitan except Australia” (Ford 1979), and is established as an introduction in the Galapagos Islands (Herring 1966; Lattin 2007a), Cook Islands (Walker & Deitz 1979), and on Easter Island (Carpintero 2002). Specimens were intercepted on Capsicum sp. arriving from Trinidad/ Tobago, and in a mail package arriving from Brazil (Table 2). Alofa sodalis may now be established as an introduction in southern Florida (FDACS 2010).

Buchananiella continua (White, 1879) is a widespread species described from the island of Madeira but of uncertain geographic origin (Lattin et al. 2001). The species commonly is found in dead leaf habitats often in association with Psocoptera and mites (Lattin et al. 2001; Aukema 2007); dead leaf habitats are commonly used by other species in this genus (Yamada & Hirowatari 2007c; Yamada & Yasunaga 2008). It has been introduced into Europe and appears to be spreading in both Great Britain and continental Europe (Aukema 2007; Rabitsch 2010). The species may also be established in Hawaii (Brenner & Lattin 2001). A female of B. continua was intercepted at the Miami airport associated with Hydrangea from Europe (Table 2). Buchananiella continua has been present in the western United States as an introduction since at least the late 1920s (Lattin et al. 2001).

Anthocoridae: Scolopini

The Scolopini is composed of approximately 18 genera of wide geographic distribution and with heavy representation in the Neotropics (Ford 1979; Schuh & Slater 1995; Carpintero 2002; Carpintero & Dellapé 2012). Calliodis Reuter, 1871, includes at least 12 species distributed almost exclusively in the New World tropics (Carpintero & Dellapé 2012). Biology of this group is relatively poorly known, although members of the genus have been collected beneath bark, in dead or dying trees, and in dead leaf habitats, where they are likely to be predaceous on small soft-bodied arthropods (Kelton 1978; Lattin 1999b; Ulyshen et al. 2012). Calliodis pallescens (Reuter, 1884) is distributed throughout Central America, South America, and the West Indies (Champion 1900; Ford 1979; Carpintero 2002; Carpintero & Dellapé 2012), and was intercepted on 3 separate shipments from these regions (Table 2). There is no evidence that this species currently occurs in the United States (Lattin 2001).

Anthocoridae: Xylocorini

The Xylocorini includes only a single genus, Xylocoris Dufour, 1831, of cosmopolitan distribution and comprising about 50 described species (Ford 1979). Species of Xylocoris occur in stored products, in granaries, in manure heaps, beneath the bark of trees, and in nests of birds (Carayon 1958; Kelton 1978; Lattin 2000; Yamada et al. 2006), and are commonly introduced into new geographic regions through transport of food products or other commodities (Southwood & Leston 1959; Carayon 1961; Herring 1967; Palta 2012). Ten specimens of 2 identified species and one unidentified species were found in interceptions (Table 2). Specimens were found in association with unidentified plants, personal effects, and “tiles”, from 2 zoogeographic regions (Table 2); marble and ceramic tiles are a common source of insect interceptions at U.S. seaports (Work et al. 2005; McCullough et al. 2006). Xylocoris afer (Reuter, 1884) occurs in subSaharan Africa, South America, Central America, Europe, Australia, and Israel (Ford 1979; Péricart & Halperin 1989; Péricart 1996; Carpintero 2002). The species has not been reported in the literature as occurring in the U.S. (Henry 1988), although we have now collected it in south Florida (in 2001, by sweep net; TTD unpublished), and in Weslaco, Texas (in 2012, on sticky traps placed in potato fields; TML unpublished). Xylocoris flavipes (Reuter, 1875) is a common predator of stored grain insects (Lattin 2000). This species is a common interception at ports, and apparently has been widely spread by commerce (Carayon 1961; Lattin 2007b,c). Xylocoris flavipes is apparently established in Hawaii (Lattin 2005a, 2007b), and is widely distributed in the continental U.S., probably as an introduction (Lattin 2007c).

Anthocoridae: Anthocorini

The Anthocorini is composed of at least 10 genera, with strong representation in the Palearctic (Carayon 1972a; Ford 1979; Carpintero 2002). The largest genus is Anthocoris Fallén, 1814, with over 50 described species (Ford 1979). Members of this genus occur often on trees and shrubs, and are important sources of biological control in orchards (Lattin 1999a, 2000). Interceptions included 2 genera, Anthocoris (8 specimens) and a single specimen of Dufouriellus ater (Dufour, 1833). The specimens of Anthocoris comprised 4 identified species and one unidentified specimen, from 2 geographic regions intercepted on plant material (Table 2). Anthocoris albiger Reuter, 1884, is a New World species found in Central America, Mexico, and the southwestern U.S. (Carpintero 2002; Lewis et al. 2005). The insect often occurs on Prosopis (Ward et al. 1977; Lewis et al. 2005), and this plant species was the source of the single interception (Table 2). Anthocoris variipes Champion, 1901, is known from South America, Central America, and Mexico, but has yet to be reported from the U.S. Anthocoris nemoralis (Fabricius, 1794) and Anthocoris nemorum (Linnaeus, 1761) are common and widespread species in Europe, and are important sources of biological control in agriculture (Lattin 1999a, 2000). Anthocoris nemoralis was intentionally released into North America to control a psyllid pest of pears, and is now established throughout the western U.S. (Horton et al. 2004).

Dufouriellus ater is the sole representative of Dufouriellus. This genus has historically been included within the Cardiastethini, but was moved to the Anthocorini by Carpintero and Dellapé (2008). Dufouriellus ater has been found under bark in association with bark beetles or other soft-bodied prey, in stored products, and in bee hives (Southwood & Leston 1959; Kelton 1978; Arbogast 1984; Lattin 2000). The species is an established introduction in Hawaii (Lattin 2005a, 2007b) and North America (Ford 1979). A single specimen was intercepted in a shipment from Italy, associated with “tile” (Table 2).

Anthocoridae: Blaptostethini

The Blaptostethini is a poorly known group of 2 genera occurring in the Old World tropics (Ford 1979). Blaptostethus Fieber, 1860, includes 6 described species of relatively poorly known biology from the Asian/African tropics (Ford 1979; Yamada 2008a). Members of this genus have been found in dead plant habitats, in nests of birds, in stored grains, on living plants, and in agricultural fields (Carayon 1958; Tawfik & El-Husseini 1971; Rajasekhara 1973; Yamada 2008a; Kaur & Virk 2011). Interceptions included 1 unidentified species from Ghana associated with “wood” (Table 2).

Lyctocoridae

The Lyctocoridae is composed of 2 genera (Ford 1979), including the geographically widespread Lyctocoris Hahn, 1836. These insects are often found in stored products, beneath bark, in manure piles and chicken houses, in nests of birds and small mammals, and in dead vegetation (Southwood & Leston 1959; Lattin 2000, 2007b). One species, Lyctocoris campestris (Fabricius, 1794), known as the “debris bug”, appears to be almost cosmopolitan in distribution, apparently because of unintentional introductions (Lattin 2007b; Rabitsch 2010). Port interceptions included 9 specimens of unidentified species from 2 zoogeographic regions associated with plants and cut flowers (Table 2).

Lasiochilidae

The Lasiochilidae is a poorly studied group of 10 genera with a strong presence in the Neotropical region (Carayon 1972a; Ford 1979; Carpintero 2002). Lasiochilus Reuter, 1871, includes nearly 50 described species associated primarily with the Neotropics and Pacific Islands (Herring 1967; Ford 1979; Carpintero 2002; Yamada & Hirowatari 2005). Members of this genus are collected from dead plant material, rotting logs, and decaying fruit (Blatchley 1926; Usinger 1946; Herring 1967; Yamada & Hirowatari 2005; Jung & Lee 2007). Nineteen specimens of (mostly unidentified) Lasiochilus were intercepted on shipments from Ecuador and Panama. Two specimens intercepted from Ecuador could be identified to species: Lasiochilus pallidulus Reuter, 1871 (Table 2). Lasiochilus pallidulus is widely distributed in Central America, South America, the West Indies, and the southern U.S. (Ford 1979; Henry 1988; Carpintero 2002), and is a relatively common part of the true bug fauna in south Florida (Blatchley 1926). Lattin (2007a) included it in his list of species introduced into the Galápagos. Herring (1966) reported its presence on Cook Island and the Galápagos.

Sources of Interceptions

We observed differences among geographic regions in numbers and taxonomic composition of interceptions (Table 3), probably because of the combined effects of zoogeography, types of products being shipped and tendency of those products to host these insects in the country of origin, and numbers of shipments arriving from each region. Interceptions arriving from South and Central America included several taxa not encountered in shipments from other regions, notably Scolopini (Anthocoridae) and Lasiochilidae (Table 3). Both of these groups are common in the New World tropics (Ford 1979; Carpintero 2002). Oriini (Anthocoridae) were intercepted from all regions except Asia. Nine of 10 intercepted specimens of Xylocoris (Anthocoridae: Xylocorini) arrived on shipments from Asia (Table 3). Interceptions arriving from South America and Central America were taxonomically the most diverse, with 9 genera identified in the interceptions (Table 3). The Anthocorini (Anthocoridae) are most heavily represented in the Palearctic and western Nearctic regions (Ford 1979). Nine specimens of Anthocorini were intercepted; the specimens were intercepted in shipments arriving from Europe and Mexico (Table 3).

Specimens representing 10 species arrived on shipments from countries outside of the species' listed geographic distributions (Table 4), suggesting that we identified several new country records in the interceptions. The assumption underlying this conclusion is that the commodity from which a given specimen was recovered (column 5 in Table 2) actually originated in the source country listed in column 2 of the table. This assumption is probably true for the majority of records in Table 2, with the most likely exceptions being specimens that were intercepted in passenger luggage or baggage. The majority of new records listed in Table 4 comprise geographic regions (countries) that neighbor the known geographic range of the species. More interesting are interceptions of species from countries well outside of the species' known geographic range. The most striking geographic anomalies in the interceptions were for 2 species of Cardiastethus. The first of these, Cardiastethus affinis, was intercepted in shipments from Thailand, Haiti, and Costa Rica (Table 4). Previous records for this species include only India and East Africa. Secondly, a specimen of Cardiastethus minutissimus was intercepted in baggage on a flight from Thailand. Previous records for C. minutissimus are limited to a number of Pacific Islands (Table 4).

TABLE 3.

GEOGRAPHICAL DISTRIBUTION OF INTERCEPTIONS.

TABLE 4.

LIST OF INTERCEPTED SPECIES WHICH ARRIVED ON SHIPMENTS FROM COUNTRIES NOT CURRENTLY LISTED AS PART OF THE SPECIES' KNOWN GEOGRAPHIC RANGE.