April 3, 2007
Conservation Status of the Endemic Bees of Hawai’I, Hylaeus (Nesoprosopis) (Hymenoptera: Colletidae)1
By Magnacca, Karl N
Abstract: The 60 species of native Hylaeus bees in the Hawaiian Islands are important pollinators in native ecosystems, but they have been almost completely ignored in conservation studies. The only previous assessment of the conservation status of the individual species was not based on recent collections. Here I report on conservation status of all known species, based on collections made from 1999 to 2002. Species are arranged into six categories according to degree of threat, and species considered to be threatened are discussed individually. Five species have not been collected recently from one or more islands from which they are historically known, seven are restricted to endangered habitat, 10 are considered to be very rare and potentially endangered, and 10 have not been collected recently and could be extinct. With such a high proportion of rare species and the importance of Hylaeus species as pollinators, further work on their ecology is needed.THE HAWAIIAN ISLANDS are famous for their numerous evolutionary radiations. A large number of species derived from a relatively small number of introductions is the rule for both plants and insects, due to extreme isolation from continents and other high islands (Zimmerman 1948, 1970, Wagner et al. 1990). The result is a fauna in which many higher taxa are absent, including some that dominate continental areas. The aculeate (stinging) Hymenoptera are a striking example. The native fauna contains 404 described endemic species, nearly 90% of which are derived from only three introductions: Hylaeus (Nesoprosopis) bees (Colletidae, 60 species), the "Nesodynerus" group of eumenine wasps (Vespidae, 112 species), and Sierola bethylid wasps (Bethylidae, 180 species with many more undescribed). The remainder includes a second small group of eumenines (the Odynerus nigripennis group, probably belonging in Euodynerus, three species), another group of bethylids (Sclerodermus, 17 species), and two Crabronidae: one group of crabronines (Ectemnius, 20 species) and two sister genera of pemphredonines, Deinomimesa and Nesomimesa (five and six species, respectively, derived from a single introduction [Nishida 2002, Daly and Magnacca 2003]). Entirely lacking are ants, social vespids, and the enormous array of other solitary hunting wasps and bees. The groups that are native to Hawai' i make up a small fraction of the fauna in continental areas, in terms of both numbers of species and numbers of individuals. For example, of the more than 3,000 species of bees in North America, there are only 48 Hylaeus species (fewer than occur in Hawai'i), distributed among seven subgenera. Moreover, the radiation in Hawai'i is extraordinary for the genus; with the inclusion of the eight known Japanese species, Nesoprosopis is the second largest subgenus of Hylaeus (Michener 2000) (the Australian subgenus Prosopisteron is also larger when undescribed species are included, but it is highly polyphyletic [unpubl. data]).
The 60 Hawaiian Hylaeus species arose from a single introduction, probably from Japan or East Asia where other species of the subgenus live (Hirashima 1977). Being strong fliers, they have a lower rate of endemism than most Hawaiian groups; only 40 of the species are single-island endemics, and many species found on Maui Nui are shared among two or more islands (Figure 1). Nevertheless, they form one of the larger Hawaiian insect radiations (Liebherr 2001). They were considered by Perkins (1913:lxxix) to be "almost the most ubiquitous of any Hawaiian insects." Unlike nearly all other native groups, they can be found across virtually the entire range of rainfall and elevation in the Islands and in all vegetation types (Figures 1 and 2). Yet despite the widely recognized importance of bees as pollinators (Proctor et al. 1996), their role in maintaining the health of Hawaiian forests and other ecosystems has not been investigated. Only recently has the basic taxonomy been revised for the first time in over 100 yr (Daly and Magnacca 2003).
Very little has been done on conservation assessment for these bees. Information is so scattered that a paper recently appeared in a major journal stating that almost the entire group was extinct (Cox and Elmqvist 2000). Thirty-four currently recognized species were listed en masse as Category 2 candidate endangered species in 1984 (see Table 1) (U.S. Fish and Wildlife Service 1984), meaning that they are likely to be endangered but that not enough information was available to justify listing as endangered. This candidate listing was based on a very preliminary assessment of conservation needs (Gagn 1982), and further determinations of listing status were made with little solid information. Eight names now considered synonyms were also included in the Category 2 list, and 17 species were listed as Category 3A (probably extinct). Five of the latter group are now considered synonyms of species known to be extant and eight have been recollected recently, but four (H. finitimus, H. mauiensis, H. melanothrix, and H. perspicuus) have still not been recovered (Daly and Magnacca 2003). Since that original listing, virtually no follow-up work has been done to ascertain the true status of the Hawaiian bees. The impetus to do so has declined even further since the Category 2 candidate list was eliminated and its members reclassified as "species of concern," with no official federal status (U.S. Fish and Wildlife Service 1996).
In this paper, I present a summary of the distribution and abundance of Hawaiian Hylaeus species, based on recent and historic collections. Rare species are considered individually, followed by discussion of factors influencing their distribution and abundance. It is intended as a first step toward assessment of the state of Hawaiian bee populations and cannot be regarded as comprehensive while several large areas of the Islands remain unsurveyed. Nevertheless, it is the first report of threats to Hylaeus species to be based on recent field data.
MATERIALS AND METHODS
Bees were collected from all main islands during the summers of 1999-2002. Collecting was done primarily with a net at flowers or over ground; at some localities yellow pan traps were used. An attempt was made to collect from all ecosystems where Hylaeus species are likely to occur. Due to a number of restrictions, collections could not be made at some sites. These restrictions included physical access, land ownership, weather, and time. Bees are also capable of maintaining populations in small areas, and sites that are largely dominated by exotic vegetation may still harbor Hylaeus species in pockets of native habitat. No collections have been made on Ni'ihau (except the islet of Lehua), offshore islets, or the Northwestern Hawaiian Islands for several decades; among the latter, Hylaeus species are recorded only from Nihoa. Additional records from other collectors were also examined; details of collection records used in this study can be found in Daly and Magnacca (2003). Unless otherwise cited, factual references here are from that reference or from personal experience.
For the purpose of conservation status analysis, the species were sorted into six categories. Placing species into discrete categories as done here is somewhat subjective but is necessary as a first step in assigning priorities. Because there is a gap of approximately 70 yr in regular collections of Hylaeus species in Hawai'i and much is still unknown about their distribution and abundance, it is difficult to use more objective categories such as those used by the IUCN (2001). The categories are (in order of increasing threat): (1) uncommon to abundant, widespread, habitat relatively safe; (2) generally found in low numbers but widespread, with a large potential habitat; (3) abundant in some areas, but some populations threatened; (4) abundant where found but habitat restricted and/or threatened; (5) very rare, potentially endangered; (6) not recently collected, probably endangered or extinct. Species in category 1 are considered to be safe, barring a dramatic increase in habitat destruction, and are not discussed. Those in categories 2 and 3 are probably safe, at least as a species, and are covered briefly. Category 4 species are discussed in the context of their habitats, which also include some category 5 species. The remainder of the category 5 and 6 species are considered individually.
The distributions and conservation status of Hylaeus species are listed in Tables 1 and 2. In addition to those shown, H. flavifrons is known from Ni'ihau (including the islet of Lehua), and H. anthracinus and H. assimulans are known from Kaho'olawe (all recent collections). The only species recorded from the Northwestern Hawaiian Islands, H. perkinsianus, is endemic to Nihoa. Little collecting has been done there, and the most recent specimens date from 1964 (Beardsley 1966). The island's vegetation appears to be largely intact, including as major components several plant species that are rare on the main islands (Conant 1985), and H. perkinsianus is probably safe. No bees were collected during a recent trip to Nihoa to assess the impact of an outbreak of Schistocerca locusts (S. Montgomery, pers. comm.), but bees in o\ther localities have been observed to go through boom-and-bust cycles. Although the locusts had a severe impact on the island's vegetation, a later trip found a low population of them and the vegetation recovering.
Figure 2 shows recent collection sites and approximate extent of habitat; empty areas of native habitat indicate regions that have been searched inadequately or not at all. Native habitat is generally patchier in reality than depicted on the map. This is particularly the case for regions on the island of Hawai'i such as South Kona where ranch land alternates with state forest reserves in maukamakai strips, and upper areas of Mauna Loa that are largely bare rock but contain numerous kipukas, "islands" of older substrate with more-developed vegetation than the surrounding, newer lava flows. On older islands, high ridges with native vegetation alternate with valleys that are often dominated by exotic plants.
Rare but Widespread
The species in this category have been collected only in low numbers and could potentially be threatened but due to the relatively large available habitat probably occur in much larger populations than collections indicate.
Hylaeus hirsutulus from Kaua'i; H. angustulus from Maui Nui; H. kukui from Maui and Hawai'i; H. crabronoides, H. filicum, H. muranus (= insignis), and H. rugulosus from Hawai'i; and H. specularis from Hawai'i, Moloka'i, O'ahu, and Kaua'i (and probably Maui) have all been collected only sporadically. All are found in wet forest (several also occur in mesic areas), and all except H. muranus are known from widely separated locales.
These species are found in habitat that is difficult to access as well as difficult to collect bees in; wet forest makes up the bulk of the areas that have not been surveyed (aside from vast areas of montane shrubland on the island of Hawai'i [Figure 2]). Because Hylaeus species typically forage only during sunny weather, the chances of successfully collecting them in these almost perpetually cloudy regions are low, and it is a testament to their adaptability that they are able to persist in such places. Thus, although they have been collected only rarely, the fact that their habitat is largely unsurveyed and is relatively pristine over large expanses (Cuddihy and Stone 1990) suggests that they may be much more abundant than their collection records imply. Although H. angustulus has not been found recently on Lana'i, that is probably due to poor weather during collecting trips and it likely persists on the island.
Hylaeus kokeensis, a newly described species from Kaua'i, appears to be restricted to mesic and dry forest. Both of these area types are generally under greater threat from development, agriculture, and invasive plants than are wet areas. However, the species occurs in a protected area (Koke'e State Park/Napali- Kona Forest Reserve), and the habitat is intact over relatively large areas. Although it has been collected only twice, it was found in high numbers. Invasive exotic plants are probably the greatest threat to this species.
Some Populations Threatened
Hylaeus connectens, though usually not greatly abundant, is the most widespread species in the Islands. It occurs on all the main islands and in all habitats except subalpine shrubland, though it seems to prefer mesic forest. Nevertheless, it has not been collected recently from Moloka'i. The habitat it is typically found in on Maui-open 'ohi'a-uluhe wet forest, with abundant Scaevola gaudichaudiana shrubs-is relatively common on Moloka'i. On other islands (Hawai'i and Kaua'i, in particular) it tends to be collected as scattered individuals, so it is not entirely surprising that it has not been found on Moloka'i. Only one collection is known from the island, so it may never have been abundant there. It is unusual, however, that it is quite abundant on O'ahu, where many other bee populations are depleted. Unknown species-specific factors are also likely at work: H. fuscipennis is abundant on Moloka'i but is now absent from O'ahu (see later in this section), although H. unicus is common on both islands, and all three occur sympatrically on Maui.
Hylaeus flavipes is the only coastal species with large, widespread populations, particularly on Hawai'i. At least in part this is because it can also be found in some upland areas; the largest known population is at the coast at South Point, but it is relatively abundant at Kipuka Nene in Hawai'i Volcanoes National Park, at approximately 900 m, and on the western slope of Mauna Kea at 1,700-2,800 m. The Maui and Lana'i populations were originally described as H. blackburni and can usually be distinguished from the Hawai'i populations by their smaller size and more extensive coloration. The initial Maui site was the Wailuku sandhills (see discussion of coastal areas in the next section); it has not been collected on Maui since 1912. It was recently rediscovered on Lana'i at an elevation of about 450 m, but the size and stability of the population there is not known. The Lana'i site is in a heavily eroded, largely barren area on the windward side of the island, in a small patch of Myoporum trees. Although other such patches presumably occur, the bees were not found on other Myoporum nearby. The coast of Lana'i has not been adequately explored for bees, but H. flavipes was not found in a small area of native vegetation at the coast where H. longiceps was present.
Hylaeus fuscipennis, like its close relative H. pubescens of Hawai'i, is one of the most common wet-forest bees of Maui Nui. It can be found there in mesic forest and even in relatively marginal habitat at the edge of native forest but has not been collected recently on O'ahu. Why this should be, when several other wet- forest species (H. connectens, H. mimicus, and H. unicus) have been collected in good habitat there, is not clear.
Hylaeus laetus is a dryland species and is also very abundant on some islands but rare on others. The only species besides H. connectens to occur on all the main islands, it is common on Hawai'i, Lana'i, and Kaua'i, even in relatively poor habitat (i.e., low plant diversity, high cover of invasive exotics, few other Hylaeus species). On Maui it has been collected recently only from a few lowland areas of West Maui, and on O'ahu from a single locality in the northern Wai'anae Range; no recent collections have come from Moloka'i. Unlike its close relatives H. difficilis and H. hirsutulus, it is almost never found in wet or even mesic forest, and this may be a primary reason for its rarity on Maui, Moloka'i, and O'ahu, where intact native dry forest and shrubland are scarce. However, all three islands have unsurveyed areas that may support larger populations of H. laetus.
Hylaeus volatilis is one of the five cleptoparasitic species of Hawaiian Hylaeus, the only known cleptoparasitic colletids (Michener 2000). It is fairly common in the subalpine shrubland in and around Haleakala National Park, where its presumed hosts, H. difficilis and H. nivicola, form extremely dense populations. Although it has historically been recorded from various parts of all the islands of Maui Nui and from O'ahu (Perkins 1899), the only other recent collection is from West Maui, above Lahaina at about 600 m. As noted earlier, other dry areas are highly degraded, although some of those that remain have not been surveyed.
Restricted to Rare Habitats
Coastal strand habitat (Figure 3) is the most endangered in Hawai'i for a number of reasons: it is highly valued for development, popular for recreation, typically dry and therefore vulnerable to fire, susceptible to invasion by exotic plants, and it covers a small area by definition. On most of the Islands, only one coastal site with diverse native vegetation is protected, making the bees that inhabit them vulnerable to single catastrophes. As a result, they make up the bulk of the areas of concern for species in this category.
At Polihale, a state park on the western coast of Kaua'i, the vegetation is almost all native along the first few banks of dunes before changing to mostly exotic trees about 100 m back from the water. The bee fauna consists of H. chlorostictus, H. connectens, H. hostilis, H. flavifrons, and H. solaris. The first three are also found in montane areas, but the last two are apparently restricted to the coast. The site is open to the public for camping and other recreational activities, making it vulnerable to physical destruction of plants by people and vehicles. However, the Pacific Missile Range Facility at Barking Sands is directly to the south and probably also includes intact habitat. There are also areas on the southeastern coast where native vegetation persists, but these are threatened by development.
Ka'ena Point, on the western tip of O'ahu, is a state Natural Area Reserve. The bee fauna includes H. anthracinus and H. longiceps; this is the only known locality for these species on O'ahu. However, H. assimulans and H. volatilis, both previously recorded from the leeward coast of O'ahu, are notable in their absence from such prime habitat. Illegal off-road driving has long been a problem there, but the site is now blocked off, and the diverse vegetation is recovering and being restored (B. Gagn, pers. comm.).
South Point (Ka Lae) is the best coastal site for bees on Hawai'i. Most of the species found there-H. anthracinus, H. difficilis, H. flavipes, H. ombrias, and H. sphecodoides-can also be found at other sites, either farther east along the coast or at higher elevations, but South Point is the only place where all the coastal species on the island (with the exception of H. psammobius) are found together. Much of the area is under the jurisdiction of the Department of Hawaiian Home Lands, but access is largely unregulated. Although driving may injure vegetation, the native plants extend over a wide enough area that the bee populations there are probably notthreatened. However, H. anthracinus appears to be restricted to regions of more-recent lava flows east of the point, on flowers of Scaevola and the introduced Tournefortia. It is not clear why this should be when the other species are abundant on the carpet of Sida ('ilima) and Jacquemontia (pa'u o Hi'iaka) growing on the older substrates and H. anthracinus is found at these plants on other islands. However, the high degree of genetic divergence between island populations of H. anthracinus (Magnacca and Danforth 2006) may point to behavioral differences between them.
A second population of H. anthracinus was recently discovered at Puhili Point on the Kona coast of Hawai'i, also on Tournefortia. Although the extent has not been fully investigated, it appears to live in a narrow area between a population of Anoplolepis gracilipes ants to the south and barren lava to the north. In addition, this area may be developed in the near future. Hylaeus difficilis, but apparently not H. anthracinus, can be found in the protected Kaloko- Honokohau National Historic Park just to the south. The difference in distribution between the two species may be related to greater ant tolerance by H. difficilis.
Mo'omomi, on the northwestern coast of Moloka'i, is a Nature Conservancy of Hawai'i preserve. Like Polihale, it consists of a native beach flora backed by mostly exotic trees. The bee fauna includes H. anthracinus and H. longiceps, as well as the extremely rare cleptoparasite H. hilaris. The latter has been collected only twice in recent years (with only a single specimen each time), and its apparent extirpation from Maui and Lana'i leaves this as the only known site for it. Based on the few visits I have made, it is difficult to estimate numbers of the other two species, its presumed hosts. However, I have never caught more than 10 bees in an hour, a much lower rate than at most other sites. The population of H. hilaris must therefore be extremely small, and among species that have been collected recently it is probably the most endangered. It is the most colorful of the Hawaiian bees: the abdomen is largely red, with unusual white hair bands, and the front of the male's head is almost entirely yellow. As one of only five species of parasitic Colletidae in the world (the others are also Hawaiian but are not threatened), it would be a particularly tragic loss if it were to become extinct. Even with a well-protected site, the apparent lack of a second population (it is unknown how far H. hilaris and its hosts extend along the coast) makes the known population highly vulnerable to fluctuations in host numbers, which can drop very low during periods of drought or other poor flowering periods.
The Kalaupapa peninsula on the northern coast of Moloka'i has an extensive area of native coastal vegetation on its east side. It is similar to the site at South Point, with prostrate, windswept plants including Chamaesyce degeneri ('akoko), Heliotropium spp. (hinahina), Jacquemontia, and Sida, as well as Tournefortia in places. Hylaeus anthracinus and H. facilis have been collected there on the latter; H. longiceps and possibly H. hilaris are probably also present on the native species during flowering season but were absent when I visited during a dry period.
There are few coastal sites of the quality of those just described on the island of Maui. Areas of native vegetation exist on the northern coast of West Maui (F. Warshauer, pers. comm.) but have not been investigated. Perkins' primary site for coastal bees on Maui was the Wailuku sandhills, which once supported a diverse bee fauna: H. anthracinus, H. assimulans, H. facilis, H. flavipes, H. hilaris, H. laetus, H. longiceps, and H. volatilis (Perkins 1899). These dunes are now built upon or covered with the exotic tree Prosopis pallida (kiawe); native plants are scarce, and bees are absent. Hylaeus flavipes and H. hilaris have not been collected on Maui since 1912; their absence from areas where other coastal or lowland species have been collected suggests that they may have been extirpated.
Two of the species listed above, H. facilis and H. volatilis, are (or were) commonly found at higher elevations. The other more strictly coastal species, H. anthracinus, H. assimulans, and H. longiceps, have been found recently at a few scattered sites around the island. The first has been collected at Kanaio at 600 m on the lower southern slopes of Haleakala, an unusual location for this otherwise exclusively coastal species (it was also found at the coast nearby, at Manawainui). Hylaeus assimulans was found in dry forest at 600 m on the western side of the island, together with H. laetus and H. volatilis. A small population of H. longiceps occurs at Waiehu, on a very small (
Hylaeus psammobius, known historically from Maui and Hawai'i, is the only native bee to inhabit windward coastal regions. It lives in Sesuvium ('akulikuli) herbland (Gagn and Cuddihy 1990), where it collects pollen of Sesuvium, Bacopa, and Lycium (unpubl. data). This is a unique habitat for a Hawaiian Hylaeus species, very different from that of other coastal species. Phylogenetic data (Magnacca and Danforth 2006) show that it is sister to H. anthracinus + H. flavifrons. Very few historic collections are known, and it has been found recently at only one site, at 'Eleilei Point on the northern coast of East Maui (similar sites exist elsewhere along the coast but have not been surveyed). Although it is reasonably abundant there, the area is so small and close to the shoreline-the plants grow on rocks barely above the spray zone, in an area ~10 m wide between the ocean and cliffs-that a single large storm could seriously damage or destroy the site as habitat for the bees. The species has not been collected on Hawai'i since 1908, but the windward coast there should be checked for intact habitat of this type.
Coastal habitat is even scarcer on Lana'i. Two of the typical coastal species, H. flavipes and H. longiceps, are primarily found at middle elevations (around 300-450 m); H. anthracinus has not been collected there recently.
A number of other potential coastal sites that have not been investigated should be checked for Hylaeus populations. These include Keoneloa on Kaua'i, Kahuku on O'ahu, and the northeastern coasts of Maui and Hawai'i. Bees have also been collected on Kaho'olawe (H. assimulans in 1997 and H. anthracinus in 2002), but the island has not been searched widely.
The most notable threatened habitat in montane regions is Chamaesyce olowaluana ('akoko) trees in mesic or dry forest in western Hawai'i. At both Pohakuloa Training Area and Pu'u Wa'awa'a Wildlife Sanctuary, isolated trees of this species appear to support large populations of a diverse group of bees rarely found elsewhere. These include H. akoko, H. dimidiatus, H. filicum, H. hula, H. kona, and H. paradoxicus, along with more common species such as H. coniceps, H. difficilis, H. laetus, and H. pele. The species of the first group were not found at nearby, more common flowering plants, such as Bidens, Myoporum, and Styphelia, where those of the second group were collected. Moreover, of the first group, only H. dimidiatus and H. paradoxicus were found at both sites, and none was found in the Mauna Loa-Mauna Kea saddle or Mauna Kea north slope regions, where C. olowaluana is more abundant. This suggests that conservation of C. olowaluana in the Pu'u Wa'awa'a and Pohakuloa areas is important for the survival of the bees, even if other populations of the tree remain. Despite abundant seed set and germination, reproduction of C. olowaluana is impeded by sheep, which devour the seedlings before they have a chance to grow.
In addition to the presence of C. olowaluana, Pohakuloa and the adjoining western slope of Mauna Kea are unique upland sites for H. flavipes and H. ombrias. Most of the other sites for the former are below 400 m, and all (except the Halepohaku record) are below 1,000 m; the only other recent collections of the latter are from South Point, at the coast. Why both species should occur there, at over 1,700 m and on an entirely different set of host plants, but not in other upland areas is unknown. It may be that the ''coastal'' species also formerly inhabited all areas of upland dry forest but not the shrubland that makes up most of the dry habitat that remains today. This would also explain the presence of H. anthracinus in dry forest at over 600 m at Kanaio on Maui, when it is otherwise strictly coastal. A single H. anthracinus was recently collected at Pohakuloa, but the existence of a viable population there still needs to be verified.
Hylaeus akoko, H. hula, H. kona, and H. paradoxicus were discussed earlier. All four might be found farther south in the uplands of the Kona and Ka'u Districts, but much of that area has been heavily grazed and has not been searched for bees since Perkins at the turn of the last century. Aside from Pu'u Wa'awa'a, H. hula is known from a small area of mesic forest at Kilauea but is rare there as well; the other species have been collected recently only on C. olowaluana at Pohakuloa or Pu'u Wa'awa'a.
Hylaeus assimulans is a large coastal and lowland species, known historically from O'ahu, Maui, Kaho'olawe, and Lana'i. It is strange that it does not seem to occur at Ka'ena Point, the best coastal site on these islands. Recent collections have been sporadic and few, from West Maui, Lana'i, and Kaho'olawe. Like its sister species, H. ombrias of Hawai'i, it appears to be more closely associated with Sida than other species are, visiting it for both nectar and pollen. Thus, it may be more common in areaswith large amounts of Sida, for example, the Prosopis (kiawe) forests of southern Lana'i. Unfortunately, I visited this area during a prolonged drought during which nearly all of the Sida had died. I collected only a few H. assimulans, but it may be more common under favorable conditions.
The closely related H. facilis and H. simplex present a striking case. According to Perkins (1899), they were among the most common and widespread species on O'ahu/Maui Nui and Hawai'i, respectively. Dozens of specimens in the Bishop Museum collection attest to this. But between the 1930s, when collecting of Hylaeus species tapered off, and recent years, when it picked up again, the species virtually disappeared. Only three specimens of H. facilis have been taken in the last 30 yr: one from O'ahu in 1975, one from Maui in 1993, and one from Moloka'i in 2005. I was unable to recover either species during extensive searches in areas where they had previously been recorded. It is a mystery why these two formerly abundant species should have decreased to the point of near extinction while substantial habitat remains and other similar, closely related species, such as H. chlorostictus and H. difficilis, are still very abundant.
The answer may be complex. It may be that H. simplex was never as common as it was thought to be. The expansion of the male gonocoxae is the primary character that unites H. simplex and H. facilis, and it is the only reliable means of distinguishing them from H. difficilis (females of the three species cannot be separated at all). The genital capsule is usually retracted within the abdomen, and the gonocoxae are not visible in most of the museum specimens labeled as H. simplex that I have examined. This makes their determinations questionable, especially in light of the current great abundance of H. difficilis. It is still strange that it should have disappeared while its habitat seems to remain but perhaps not as much so as if it had been very abundant.
The gonocoxae of H. facilis are usually visible externally even without being extracted, and there is no question that it was formerly quite common. However, all dry- and mesic-forest species are now rare on Maui Nui and O'ahu. Even H. laetus, one of the most common species in drier areas of Kaua'i and Hawai'i, is difficult to find on Maui and O'ahu, and has not been recently collected on Moloka'i. Native dry and mesic habitats have been decimated on the latter three islands (Mueller-Dombois 1973, Medeiros et al. 1986); much of what remains is in very small patches that may be incapable of supporting a population of bees. It may be that if H. facilis still survives on Maui and O'ahu, it is in small remnant patches of mesic or dry forest that have yet to be searched for bees.
Two recently described O'ahu species, H. kuakea and H. mana, are also inhabitants of mesic forests. Each is known from a single collection record, with two and four specimens, respectively. The former is from a Nature Conservancy preserve in the Wai'anae Range (Honouliuli); this region contains a relatively large amount of potential habitat, and current protection and restoration efforts may help maintain it there. It is not known what its specific habitat requirements are. Hylaeus mana was collected in mesic forest on Santalum at a relatively low elevation (430 m) in the leeward Ko'olau Range. Although there is a considerable amount of native wet forest above 500 m, at lower elevations and rainfall levels the vegetation is largely alien on most of the ridges with trails. That no other species were found with either H. kuakea or H. mana, and both were collected more or less by accident, suggests that more intensive and systematic searching will turn up more specimens and possibly even more species. Nevertheless, the fact that it has taken so long for them to be discovered, coupled with the general scarcity of their habitat, means they are likely to remain rare.
Ten species have not been collected recently, including the previously mentioned H. simplex. Most are known from very few specimens.
Hylaeus anomalus occurred on southern leeward Ko'olau ridges on O'ahu. Although apparently never highly abundant, it was not uncommon during the early collecting period through the 1930s. Like H. fuscipennis, which lived in the same area, it has not been collected in decades. In light of the apparent disappearance of these two species from the area, it is particularly strange that the newly described H. mimicus had not been collected before. Even on the ridges directly above Honolulu, I found the latter species in sufficient numbers that a collector could hardly fail to recover it; yet in the Bishop Museum collection (which contains dozens of H. facilis from this area) only a single specimen was found, and that was from the northern Ko'olau Range where little collecting was done. Clearly a shift in species composition has occurred in the area despite the apparently good quality of the vegetation.
Hylaeus finitimus is known from two specimens collected by Perkins (1899) on the coast at Makaweli (probably in the vicinity of Ho'anuanu Bay, east of Waimea) on Kaua'i. Although there are patches of Scaevola at the coast in that area, there do not appear to be any intact coastal communities there. Perkins (1899) stated that he searched there and in other places for more specimens and did not find any, and the species was not found at Polihale. Whether it is phylogenetically closer to H. longiceps or H. flavipes is uncertain because the male specimen cannot be located; Perkins' description (1899) and later key (1910) are in conflict regarding the characters that separate H. finitimus from the other two. The female is indistinguishable from H. longiceps, and it may simply be a Kaua'i population of that species.
Hylaeus gliddenae is known from a single male collected at Kilauea in 1934. Its habitat is unknown, but the label states that it came from a nest burrow in Myrsine, a tree that is widespread but most common and largest in mesic forest. Its obvious close relationship to H. paradoxicus, a mesic- or dry-forest species, supports this conclusion. In fact, it is conceivable that at least some of the smaller, rare females described by Perkins (1899) as H. erythrodemas (a name later synonymized with H. paradoxicus) were actually females of H. gliddenae. Kilauea straddles a steep rainfall gradient, so wet, mesic, and dry habitats can be found within a few kilometers (Figure 2). It has also been protected as part of Hawai'i Volcanoes National Park since 1916. As a result, it is the most diverse locality for bees: 22 of the 28 Hawai'i Island species have been collected there, all except four coastal species and two that are confined to Kona. Eighteen of the 22 have been collected at Kilauea recently, but several mesic- to dry-forest species, including H. paradoxicus, have been found exclusively or more abundantly at localities in northwestern Hawai'i such as Pu'u Wa'awa'a and Pohakuloa. It therefore seems more likely that H. gliddenae will be found at these sites than at its type locality.
Hylaeus nalo is also known only from a single male, collected on O'ahu in 1914. The specific locality is not recorded on the label, and it does not show any clear affinities to other species. The most likely sister species is probably H. rugulosus, although there are several other possibilities. The lack of information about it obviously makes it hard to search for, which is especially frustrating in light of the difficulty in interpreting its relationships and its unique morphology. It is a large species, but its impunctate metasoma and broad scape separate it from the other groups of large species (the pubescens group, and H. assimulans and H. ombrias, respectively). It also possesses truncate gonocoxae, which are unique in the subgenus, and peculiar, poorly defined facial marks.
Hylaeus mauiensis, H. melanothrix, and H. satelles are all recorded from wet forests of Maui (the last has also been collected on Moloka'i and Lana'i). The first is known from only a single male (the female was described by Perkins , but the specimen could not be located); modest series of the other two exist. All three were collected from very wet areas that are difficult to access and to collect in, so it is not surprising that they have not been collected recently. Large areas of intact wet-forest habitat remain on the island, so more-intensive collecting will probably turn up these species.
Hylaeus niloticus (= obscuratus) is known from a few specimens collected on the coasts and lowlands of Hawai'i, Lana'i, and Moloka'i. Little or no native habitat remains in the areas where it was collected previously (Kona coast of Hawai'i, dry lowlands of Moloka'i), and it has not been found in similar areas where other coastal Hylaeus species have been collected (e.g., South Point, Pohakuloa, Mo'omomi). A few other areas of native dry habitat remain, such as at Kamiloloa in central Moloka'i, but have not been searched.
Hylaeus perspicuus is known from a few specimens collected by Perkins in mesic to wet forest at Makaweli on Kaua'i. This area is privately owned and has not been surveyed for bees recently, and the species has not turned up in similar habitat around Waimea Canyon and the Alaka'i region. Still, the wetter areas east of the canyon where it is most likely to be found have not been searched intensively, and it is also possible that it is limited to the Makaweli area.
Vegetation and Habitat
The strong dependence of all species of Hylaeus on native plants to the near-complete exclusion of exotics (with the sole exception of Tournefortia among the latter) means that to conserve them native forests and shrublands must be preserved. Conservation of the plants and bees is a reciprocal situation, given the likely status of Hylaeus species as primary pollinators of many impor\tant plants. Based on current distributional information, it is clear that for bees to be present, at least some level of vegetation diversity is required. This is probably due to a combination of temporal (i.e., year-round availability of floral resources) and nutritional factors. Visitation records (Daly and Magnacca 2003) and identification of pollen loads (unpubl. data) indicate that Hylaeus species are frequent visitors to many of the community-dominant plants of Hawaiian ecosystems. All of the top 10 pollen types collected by Hylaeus species are the dominant or codominant plants in wet forest or dry or coastal shrubland (Table 3, Favored flowers). In addition, several rare species are regularly visited where they are found (Table 3, Rare plants). Although pollination rates have not been investigated, for many of these plants Hylaeus species are almost the only regular floral visitors and are undoubtedly important for native plant reproduction and hence ecosystem health.
Dry and mesic forests seem to be an exception to the dominant- plant rule. Aside from Metrosideros, most of the dominant trees characteristic of dry and mesic forest (Table 3, Dominant dry- forest trees) are not attractive to bees; many of those that potentially are attractive, such as Reynoldsia sandwicensis (Araliaceae, 'ohe makai), are now rare. Only Sophora, which is abundant in montane dry forest on Maui and Hawai'i but relatively rare on the other islands, and Myoporum, which has a similarly patchy distribution, are commonly visited dryland trees. Although it is a favored plant in all habitats, Metrosideros appears to be incapable of supporting bees on its own; they are rarely found where Metrosideros is the only native flower available. Instead, Hylaeus species primarily visit understory shrubs such as Dodonaea and Styphelia. As a result, composition of the flora, not merely diversity, is probably a major constraint on bee populations in this habitat. Although there are still some large, native dry and mesic areas on Kaua'i and Hawai'i, much of the latter is pioneer vegetation on barren lava flows, consisting almost exclusively of scattered Metrosideros ( Jacobi and Scott 1985). Even in many remaining forests with a native canopy, the native understory shrubs that form a large part of the diet of Hylaeus species are often absent due to the presence of invasive grasses and shrubs (Cuddihy and Stone 1990, Gagn and Cuddihy 1990). On O'ahu and Maui Nui, dry and mesic forest and shrubland is restricted to small patches (Figure 2) (Mueller-Dombois 1973, Medeiros et al. 1986). At least partly as a result, the middle islands have a much higher proportion of unrecovered species than do Hawai'i and Kaua'i (Table 1).
Chamaesyce olowaluana represents a striking example of the impact that only a few individuals of a preferred host can have. It is one of the most favored host plants despite its rarity and peculiar flowers, which are minute and effectively petal-less. Nine species of bees were collected on an isolated tree in remnant mesic forest at Pu'u Wa'awa'a, but there were almost none on other flowering trees nearby. Similar areas a few hundred meters away, even at sites with greater overall diversity and density of native plants, also had very low bee numbers and diversity, consisting only of common, widespread species. Another single tree in dry forest at Pohakuloa had similarly high diversity relative to nearby areas. This suggests that dry and mesic forests may once have supported many more bee species that are now extirpated because certain favored plants are gone. It also indicates that the remaining dry forests, especially those with high diversity and an intact native understory, should be searched intensively for bees, rather than passed over because a quick search finds none on the most common trees. Given the widespread destruction of dry forests and drastic reduction in diversity in much that remains, it is probable that some species of Hylaeus may have become extinct due to habitat loss before being discovered.
Coastal species face a similar situation. Although the indigenous Scaevola sericea is common and widespread, Hylaeus species are apparently not capable of surviving on it alone. Although their exact requirements are not known, coastal bees are almost exclusively found in areas dominated by a variety of native shrubs and herbs, including Chamaesyce, Jacquemontia, and Sida. Analysis of pollen loads (unpubl. data) shows that coastal species in particular use many different plants as food sources, not only seasonally but at any given time. In contrast, most native wet forests are capable of supporting bees, at least partially because the pollen diet of wet-forest species is overwhelmingly made up of only two species, Metrosideros polymorpha and Cheirodendron trigynum (unpubl. data). Both of these are usually present at relatively high frequency even in moderately disturbed forest. Despite its reputation for being gravely threatened worldwide, wet forest is the most intact ecosystem in Hawai'i (Figure 2) (Cuddihy and Stone 1990). Large expanses of forest are protected, to a greater or lesser degree, in montane areas of central Kaua'i; windward O'ahu, Moloka'i, Maui, and Hawai'i; and Kona and Ka'u Districts on Hawai'i.
The nesting habits of most Hawaiian Hylaeus species are unknown. However, many bees are more limited by availability of nest sites than host plants (Westrich 1989), and this may be the case for Hawaiian species as well. Although most Hylaeus species worldwide nest in dead pithy stems, examples of species that nest in a variety of other substrates are known (Michener 2000 and references therein). Among the Hawaiian species, it appears that those inhabiting wet areas nest in stems or wood, whereas dryland species nest in the ground. Hylaeus anomalus, H. dumetorum, H. gliddenae, H. pubescens, H. setosifrons, and H. unicus are known as examples of the former, and H. difficilis, H. flavipes, H. laetus, H. nivicola, and H. rugulosus the latter. At least some ground-nesting species are also able to nest in crevices under rocks (Cole et al. 1992) or in rock walls. The cleptoparasitic species appear to attack only ground or crevice nesters.
Hylaeus species lack modifications for digging, such as strong mandibles and a pygidial plate that would allow them to excavate solid wood and hard-packed soil. Almost certainly in the case of wood nesters, and possibly for ground nesters as well, the nest holes are usually not initiated by the bees but are the result of burrows made by other insects, such as Plagithmysus beetles (Cerambycidae) or Ectemnius wasps (Crabronidae). If this is the case, they are dependent on the abundance of other species for nest sites.
Competition with introduced bees is a potentially important factor that has not been investigated in Hawai'i. A large number of alien species have been introduced to Hawai'i over the past 200 yr, including some hymenopterans (such as ants and yellowjacket wasps) that have wreaked havoc on native arthropods (Perkins 1913, Zimmerman 1948, Gambino 1992, Gillespie and Reimer 1993). Fifteen species of exotic bees have been introduced into Hawai'i (Snelling 2003); 14 are adventive, nearly as many as in all of North America ( J. Ascher, pers. comm.). Some introduced species (Hylaeus leptocephala, Lithurgus scabrosus, Megachile spp., and Xylocopa sonorina) occur in relatively low numbers or almost exclusively in areas dominated by introduced plants and are generally not considered a threat to native species. Others, including Apis mellifera (honeybee), Ceratina arizonensis, C. nr. dentipes, C. smaragdula, Hylaeus albonitens, and Lasioglossum impavidum, occur abundantly in company with native Hylaeus species. Apis species can be found in extremely high numbers in some areas. The parasites that have decimated feral honeybee populations in North America, the Asian bee mite (Varroa jacobsoni) and tracheal mite (Acarapis woodi) (Hoopingarner and Waller 1992), are not present in Hawai'i. Apis species readily visit a wide variety of both native and exotic plants (Arita et al. 1989) and forage throughout the day and in cloudy or even rainy weather. In some areas, it seems that by sheer numbers they could hardly fail to have an impact on Hylaeus species, especially with regard to the nectar supply. The pollination relationship between Hylaeus species and the endangered plant Sesbania tomentosa at Ka'ena Point on O'ahu was studied by Hopper (2002), who found that Hylaeus species are the primary pollinators, with Apis species mainly acting as nectar robbers. Still, although abundant on Metrosideros, Myoporum, Scaevola, and Sophora, honeybees are rarely found on some of the other important pollen plants for the native bees, such as Cheirodendron, Dodonaea, and Styphelia. Although Hylaeus species do not occur in native habitat where there are large numbers of honeybees, the impact of moderate populations of Apis species is not known. The other common species, Ceratina spp., H. albonitens, and L. impavidum, are more similar in size and flower visitation to native Hylaeus species and may have a greater impact through pollen collection. All five are almost completely unstudied in Hawai'i, and only recently has their presence and/or extent of distribution been documented (Snelling 2003).
Ants are considered the greatest threat to native arthropods (Perkins 1913), but their effect on Hylaeus species is not fully known. Although Cole et al. (1992) found that Argentine ants (Linepithema humile) on Haleakala eliminated bees from ant-infested areas, they only compared the abundance of bee nests under rocks in ant and non-ant areas. It may be that bees in small burrows in sand or soil (the typical nesting medium for dryland Hylaeus species in Hawai'i) are less vulnerable than those in unexcavated nests under loose rocks. Reduct\ion or extirpation of their Hylaeus pollinators by ants and/or alien bees may have been a factor in elimination of native plants from much of the coast.
Nearly half of the Hawaiian Hylaeus species face immediate threats, primarily due to habitat loss or alteration, and 10 are already possibly extinct. As a potential keystone group in all Hawaiian ecosystems, they deserve greater study of their behavior and ecology, as well as their broader influence on native habitats through pollination. The degree of reliance of both common and rare plants on pollination by Hylaeus species, tolerance of bees for alien bees and ants, and nesting biology are all fertile subjects for future research that would greatly enhance our understanding of the role of Hylaeus species in Hawaiian ecosystems and the steps necessary for their conservation.
Thanks to Bryan Danforth, Jim Liebherr, and Pamela Scheffler for reviewing the manuscript. Funding for collecting trips came from a grant to Howell Daly (University of California-Berkeley) from the U.S. Fish and Wildlife Service, Pacific Islands Ecoregion, Ecological Services, Honolulu.
1 Manuscript accepted 5 May 2006.
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Karl N. Magnacca2,3
2 Department of Entomology, Cornell University, Ithaca, New York 14850.
3 Current address: Department of Environmental Science, Policy, and Management, University of California-Berkeley, Berkeley, California 94720 (e-mail: [email protected]).
Copyright University Press of Hawaii Apr 2007
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