- Email: [email protected]
Bee and ant burrows in Quaternary “coffee rock” and Holocene sand dunes, Kowhai Bay, Northland, New Zealand
Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Bee and ant burrows in Quaternary “coffee rock” and Holocene sand dunes, Kowhai Bay, Northland, New Zealand Murray R. Gregory a, Kathleen A. Campbell a,⁎, Andrea C. Alfaro b, Neville Hudson a a b
School of Geography, Geology and Environmental Science, The University of Auckland, Private Bag 92019, Auckand 1142, New Zealand School of Applied Sciences, Auckland University of Technology, Private Bag 92006, Auckland 1142, New Zealand
a r t i c l e
i n f o
Article history: Received 23 November 2007 Received in revised form 30 October 2008 Accepted 2 December 2008 Keywords: Bees and ants Surface mounds and burrows Quaternary “coffee rock” Palaeosols Northland New Zealand
a b s t r a c t Curious, multi-coloured, and pelleted sand mounds (tumuli) constructed by solitary bees, together with similar, but loosely piled white sand mounds made by ants, are a striking feature of deflation and erosion surfaces in coastal sand dune territory of northernmost New Zealand. These native bee and ant mounds (to N 20 mounds/m2) are found, respectively, on consolidated Quaternary “coffee rock” or atop shifting modern dune sands at Kowhai Bay, Aupouri Peninsula, across an area of several hundred square metres of bare and/or partly vegetated ground, lying some 800 m inland from the open ocean-facing Kowhai Beach. The vicinity is otherwise covered by scrubland vegetation dominated by the local ti tree, kanuka (Kunzea ericoides, var. linaris), and the aggressive introduced alien, Acacia longifolium, which bloom in spring or summer, respectively, attracting bees, ants and other insects to the area. Many of the pelleted bee mounds are connected to simple and open, vertical to steeply inclined cylindrical shafts (cf. Skolithos) that may reach depths approaching one metre. The shafts sometimes terminate in a slightly ovoidal chamber (cell) that is lined with translucent, mucoidal, parchment-like layers and/or stuffed with pollen, and which occasionally contains a single white larva. These biogenic structures are created by solitary endemic colletid bees (Leioproctus (Leioproctus) metallicus) which we observed burrowing vertically through firm “coffee rock” at rates of up to 4 cm/hour. Many of these shafts are plugged near the surface by sand (uppermost 10 cm), or dead-end at shallow depths, suggesting concealment and decoy strategies used to avoid the bees’ natural predator, parasitic gasteruptid wasps. In contrast to the pelleted and multi-coloured bee mounds, those made by ants (e.g., Monomorium antarcticum) are uniformly pale grey or white in colour, with a granular and smooth, fine to medium sand surface (i.e., they are non-pelleted). These ant mounds are crescent-shaped to circular, with a conspicuous central entrance hole that lies in a cratered depression, and which opens into irregularly branching burrows and passages that lack a lining other than some weak and discontinuous mucus-like coating (cf. Socialites). Quadrat sampling suggests that bee and ant mound distributions are oppositely related to substrate coherency. Field excavations indicate strong overprinting by bee excavations on consolidated dune fabrics. It is suggested that their burrows may have influenced groundwater movement in these iron-rich, paleosolbearing strata. They also imply a paleoenvironmental shift from Kauri forest cover to deflationary sand dune episodes in the semi-tropical climate of the late Quaternary of northern New Zealand. The terrestrial deflationary setting can be likened to omission surfaces of marine environments. © 2008 Elsevier B.V. All rights reserved.
1. Introduction: endemic bees and ants of Kowhai Bay, New Zealand Both bees and ants are elements of the depauperate New Zealand insect biota, and their taxonomy has only recently been the subject of thorough and detailed investigation (e.g., Donovan, 2007, bees; and Don, 2007, ants). There are at least 40 species of bees endemic to New Zealand, with all of them belonging to the two most primitive bee families — Colletidae and Halictidae. Of these, 36 are representatives ⁎ Corresponding author. Tel.: +64 9 373 7599; fax: +64 9 373 7435. E-mail address: [email protected] (K.A. Campbell). 0031-0182/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2008.12.008
of the former. The native New Zealand bee biota, and also that of New Caledonia 1600 km to the NNW with 28 species, are depauperate when compared with their continental Australian source where N950 species have been identified (Donovan, 1980, 1983). Typical local nesting sites for bees of the colletid family are areas of barren or semibare ground that are free from excess moisture over the late springsummer nesting season. Nests typically consist of simple tunnels or burrows which extend to depths of 20–50 cm and commonly terminate in pollen-stuffed, ovoidal cavities (brood cells) (Donovan, 1980, 1983, 1984, 2007). They feed on, and gather pollen from, local flowering plants, but in New Zealand are particularly attracted to ti trees, manuka and kanuka (Leptospermum scorparium and Kunzea
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
ericoides var. linaris), which are dominant features of the flora of northern New Zealand scrublands. Of some 37 established ant species recognized in New Zealand, 10 or 11 are generally accepted to be endemic and most of the remainder are considered recent arrivals from Australia (Waller, 1984; Don, 2007). While bee mounds (tumuli) are restricted to areas of consolidated Quaternary “coffee rock”, they share these exposed surfaces with ant mounds. The ant mounds also are persistent across broad, shifting sand-flat areas and can be followed into sand beaches for a short distance above high tide level. Excavations into loose sands and “coffee rock” generally expose galleried passages, some of which
103
can be traced laterally for distances of 2 m or more and may reach depths exceeding 70 cm. The primary objectives of this study were to further our understanding of the role played by the burrowing activities of local bees and ants in the Quaternary “coffee rock” of Kowhai Bay, and their significance in the resulting development of overprinted ichno- or pedofabrics. 2. Setting: Kowhai Bay Over Quaternary times, northwards drifting sands fed the growth of two large tombolos in the region. These have permanently linked to
Fig. 1. Kowhai Bay with sampling locality indicated by “x”; 20 m contour defines extent of ridge crest.
104
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Fig. 2. General view looking eastwards along the arcuate length of Kowhai Bay. Note the build up of a substantial sandy foredune along its length, the irregular exposures of deflationary “coffee rock” surfaces (in foreground) and vegetation cover of 20 m ridge in middle-distance.
the mainland an archipelago of once upstanding, erosion resistant islands. Aspects of the Quaternary dunes and associated “coffee rock” paleoenvironments have been described in detail elsewhere (see Gregory and Campbell 2003; Gregory et al., 2004, 2005, 2006). Kowhai Bay is a minor arcuate indention, some 2 km in length, located towards the southern end of Aupouri Peninsula (Fig. 1). It faces northeastwards into Great Exhibition Bay and is protected to the north and south by prominent basement headlands Fig. 1. The land immediately behind
Kowhai Beach, and between it and Houhora Harbour (Fig. 1), rises abruptly to a conspicuous N20 m high ridge, typified by discontinuous, deflation exposures of consolidated “coffee rock” (i.e. compacted and weakly cemented strata dominated by humates and iron oxides) and case-hardened, limonitic crusts representing older, semi-indurated sand dunes (e.g. Hicks, 1975). The exposed surfaces are intermittently covered by present-day, wind blown, white to off white, drifting fine to medium sand (Fig. 2).
Fig. 3. Numerous and varied casting mounds in drifting sand on westerly facing, irregular surface and towards 20 m ridge crest; with deflationary surfaces arrowed (a); closer view with both bee (1) and ant (2) burrow mounds indicated (b); typical bee casting mound with pelleted surface and no entrance hole evident (c); “bulls eye” pattern of changing colours that reflects a bee's sequential passage though horizons of differing colour and the local “coffee rock” stratigraphy (d) (coin diam. = 21 mm).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
3. Mound and burrow characteristics 3.1. Bee mounds — general overview The study site covers an area of several thousand square metres, and lies some 800 m inland from the easterly facing, open-ocean shoreline. Here bare, irregular and undulating deflationary surfaces, cut across consolidated older Quaternary sands (“coffee rock”). A thin and patchy cover of contemporary drifting sand, irregularly interspersed with sand mounds is a noteworthy feature of this area and is particularly conspicuous across the crest and northwest flank of a low hill (Fig. 3a). During our spring visits (November–December), the air was buzzing with activities of a local colletid native bee (Leioproctus (Leioproctus) metallicus), and an endemic, cleptoparasitoid gasteruptid wasp (Pseudofoenus crassipes; female). On three occasions in the late spring and early summers of 2002, 2003 and 2004, this surface was covered with numerous mono- and multi-hued “casting” mounds (tumuli) (Fig. 3b–d). These conical structures were generally circular, 8–10+ cm diameter in outline and 2–N3 cm in height. At, or closely near each mound's central peak, there was commonly an open “entrance” hole, 0.5–1 cm across. In many instances the mounds were
105
built of elongate rod-like “pellets” (maximum length ~ 1 cm, diameter 3–4 mm), distributed in a crudely sub-radial pattern about their centre (Fig. 3d). Typically, in the sediment pile of these mounds, there was a veritable ‘rainbow’ display — a ‘bulls eye’ effect — with concentric colour changes (white, yellow, orange, brown, dark brown, purple, dark red, and charcoal). This pattern is a reflection of the different coloured sediment horizons being encountered by each tracemaker during excavation through varying depths (to N90 cm) (Fig. 3c and d). In others, the mounds were structureless with loose sand cascading from the central peak. The former were attributed to bee burrowing activities and are readily distinguished from the latter, which were made by ant activity across the same general area (see later sections). 3.2. Bee burrows — description and construction Where there was no drifting sand cover, exposed “coffee rock” surfaces were commonly pock-marked by sharply defined, circular, smooth-walled holes, ~ 1 cm in diameter, and which extended vertically to depths reaching 10 cm. These burrows did not branch and were otherwise blind. Shallow scraping through numerous
Fig. 4. After removal of surface-drifting, loose sand cover and scraping up to 10 cm in to the buried “coffee rock”, the open circular shafts (black) made by the bee Leioproctus (? Skolithos) come into view. Fresh-filled shafts (see large arrow) and old, iron stained plugged holes (see thin arrows) are also present (coin diam. = 30 mm) (a). Schematic diagram, illustrating mound and vertical access, plugged sloping segment, and vertical shaft with ovoidal brooding chamber (b).
106
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
mounds, and removal of drifting sand cover, exposed the surface of underlying “coffee rock”. Continued scraping and gradual removal of a layer 10–12 cm thick over an area of 0.75 m2 commonly revealed a number of once “hidden”, open and vertical to steeply inclined circular shafts 8–10 mm in diameter (Fig. 4a). The upper parts of these shafts had been plugged by sand over a depth of 5–10 cm or more (Fig. 4b). Excavation and probing in the “coffee rock” have shown that some of the simple open shafts extend (more or less vertically) to depths of at least 95 cm with no intervening obstructions and bear remarkable resemblance to the ichnogenus Skolithos. Comparable bee burrowing activities are a widely reported activity in palaeosols (e.g., Stanley and Fagerstrom, 1974; Retallack, 1984; Elliot and Nations, 1998; Mikuláš and Cilek, 1998; Genise et al., 2004) and exposures of castellated sandstones (e.g., Mikuláš, 2001). Bee burrowing and shaft excavation is a seasonal activity — late spring to early summer (mid November to early January), and over the period when ti tree (manuka and kanuka) was in full bloom. After a seemingly random, if not irrational and irregular search, while flying over and sometimes landing briefly across an area of a square metre or so, bees settle on “selected appropriate” sites. There they build mounds by “cork-screwing” their way into and through a shallow layer of loose, surface-drifting soft sand. In so doing they quickly disappear from view (Fig. 5a–d). At a depth of a few centimetres they are commonly excavating into a consolidated and firm “coffee rock” substrate. Observations were made of L. metallicus bees released into a glass terrarium packed with Kowhai Beach-sourced, loose and
weakly compacted, dampened sand. These observations showed that this sediment substrate was being manipulated between the bees’ abdomen and legs and quickly “kneaded” into rod-like pellets. These pellets were pushed progressively upwards to emerge in or left exposed at the sandy sediment surface. Individual bees continued to bring forth material from depth without themselves necessarily reappearing at the surface (Fig. 5b). The process must involve liquefaction and/or fluidization similar to that described by Genise and Poiré (2000). Sequential, field observations on one day, over a period of several hours, suggest the bee-burrowing rate may reach 4 cm/h. At this rate, burrowing to a depth of 90 cm could take N24 h! Temperatures measured at the base of deep burrow shafts were 2–3 °C cooler than those of the sun-drenched surface above, and the substrate was slightly moist at depth as well. By the end of early summer (January), both adult colletid bees and the cleptoparasitoid gasteruptid wasps had mostly disappeared (see also Section 4). The bee mounds had also vanished, for these quickly disintegrate with wind and rain. In the following months (February–June) Acacia came into flower and introduced honey-bees (Apis mellifera) became numerous. Hence, the honey bee/Acacia association is temporally exclusive to the colletid bee/ti tree association in the same locale. 3.3. Brood cells Several deep vertical shafts of the bee burrows terminated at their base in a solitary, slightly expanded and ovoidal chamber. These
Fig. 5. Sequence of bee moving around and corkscrewing its way into the sand substrate before disappearing from view (a–d) and pushing a pellet to the surface without emerging (e); early mound development after three or four hours activity (f); live bee in glass terrarium, actively kneading a sandy pellet (dashed) and which was moved subsequently towards the surface (g).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
107
“brood cells” were sometimes lined with a thick and somewhat brittle, cellophane-like secretion, that probably hardens after being applied by the female's tongue (Anonymous, 2002), and also helps to keep the chamber dry from external moisture (Batra, 1984). Lower parts of some shafts were similarly lined, and slugs or pellets of pollen were occasionally encountered at the base of excavated shafts. In rare instances a solitary larval inhabitant was present (Fig. 6a–b). Short simple and rarely branching, lateral tunnels coming off open vertical shafts were uncommon and generally blind. These were never observed to open into multiple brooding cells set in sophisticated and whorled or tiered patterns of the kind associated with the ichnofamily Celliformidae. Nonetheless, Celliformidae also includes ichnogenera of simple morphology like Celliforma itself, and Palmiraichnus (e.g. Elliot and Nations, 1998, Figs. 5 and 6; Genise, 2000, Figs. 1 and 2; Genise et al., 2002, Fig. 6; Hasiotis, 2003, Fig. 3). In rare instances the termination of these short tunnels was slightly expanded and could host a pollen slug or a solitary white larva. 3.4. Ant mounds When fresh, mounds made by a local endemic ant (Monomorium antarcticum) in the same area are easily distinguished from those made by native bees. They are smooth surfaced, typically built of loosely packed, pale cream-coloured or white, surface drifting medium to fine sand, and tumuli slopes were never pelleted. These mounds typically exhibited a crudely “half-moon” crescent shape in plan view, volcanolike in cross-section, and tended to be slightly broader than bee casting mounds (Fig. 7a and b, 8a). Ant mounds typically had a central, or slightly off-set entrance hole that lay in shallow depressions that were
Fig. 7. Typical ant mounds from sand flat habitats; note the absence of pelleted surfaces and limited evidence for excavations into “coffee rock”(a, b); entrance holes are often conspicuously off-set (a) and crescentic in shape, with the mound surface sloping away from the entrance — a volcano in miniature that is beached on one side (b) (coin diam. = 30 mm).
often breached to one side. Ant tunnels are generally much smaller than bee shafts (1 mm to b10 mm). Although the diameter of some major passages may exceed 1 cm, they are often highly irregular and roughly surfaced (Fig. 8b). Very small, irregularly distributed, and generally difficult to identify entrances (unless ants are coming and going) may be present across mound surfaces. Adopting procedures developed by several earlier authors (e.g., Genise, 1979; Williams and Lofgren, 1988; Tschinkel, 2003), a number of casts have been made with an orthodontal plaster slurry (labrock or labstone). An example is illustrated in Fig. 8c. Ant colonies may have numerous minor entranceways common to a major tunnel, which leads to a complex of open irregular passages and pillared-galleries that are stacked at intervals to depths of N60 cm. These are neither as well developed nor as systematically organized as those illustrated by Tschinkel (2003, e.g., Figs. 5 and 9). Crude nesting patterns revealed during excavations (Fig. 8b) bear similarities to the ichnospecies Socialites tumulus recently described by Roberts and Tapanila (2006), and attributed by them to ant activity. Some of the major tunnels or burrows are discontinuously interconnected by finer tubular passages and have lateral sloping and/or horizontal extents of two metres or more (Fig. 8c). 4. Distribution of bee and ant burrows at Kowhai Bay Three distinctive habitats were identified across the study area. Their distribution patterns are illustrated in Fig. 9a–c. Fig. 6. Parchment-like surface lining of brood cell (a), empty pupal cell (large arrow) lying alongside its removed larval inhabitant (thin arrow, b).
1:- On the flanks and towards the ridge-crest of older and consolidated “coffee rock” exposures, the habitat was largely bare
108
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Towards the ridge crest, where most of the bee burrows were observed, 12 1-m2 quadrats were excavated to 45 cm, exposing a number of open shafts, a few of which could be traced continuously through the vertical depth of an excavation. The number of open holes (Fig. 4a), freshly sand-filled holes (defined by sharp boundaries), and old (iron stained, diffuse boundaries) filled burrows were recorded at set depth intervals (0–5, 6–14, 15–24, 25–35, 36–46 cm) during the excavations (Fig. 9a and b). The overall trend is for all burrow types to decrease in number with increasing depth. At depth, old filled burrows were about six times more abundant than the other two types. In addition, a peak in open holes was identified at approximately 10 cm below the surface in the majority of quadrats (Fig. 10). Fewer open holes at the surface, compared to those at a depth of 10 cm, may be explained by the bees’ behaviour of plugging the tops of holes through depths 0–10 cm, with the objective of concealing them from predators, such as cleptoparasitic (predatory-inquiline) gasteruptid wasps. Pseudofoenus is known to be a predator-inquiline on colletid bees (Jennings and Austin, 2002), and hence the female lays its egg upon the larva of the bee such that the emergent wasp larva consumes the pollen ball and/or the bee larva within the burrow of the bee. Thus, the temporal
Fig. 8. A shallow vertical excavation reveals white, sand-filled, irregular galleries at shallow depth beneath a “volcanic” ant mound (arrowed) (a) (pen-knife = 9 cm) and fresh, currently active and open burrows at greater depth (coin diam. = 21 mm). Other excavations have exposed substantial and open sub-horizontal galleries of varying size (b) and with numerous small vertical access paths/burrows, many of which can be traced into surface “volcano-shaped mounds”. Some of the large galleries have been traced for distances reaching N2 m. Casts were made with “labrock plaster,” introduced as a thin slurry poured into major surface entrance holes (c).
ground with a few patches of drifting sand and widely spaced scrubby plants. 2:- Distally from the ridge crest, a rippled sand flat is dominated by soft sandy substrates with minor patches of grass. 3:- Between these two habitats lies a transition zone with varying mixtures of shrub-covered ground, grassy areas and sand. Bee burrows were most abundant in extensive patches of bare ground towards the ridge crest, they were rare in the transition zone, and absent from the soft sand flat habitat, as well as missing from the open ocean-facing back beach and sandy fore-dunes. Ant mounds were present and conspicuous in all three habitats, with abundance increasing from the ridge crest (i.e., “hill” in Fig. 9) towards the sand flats (Fig. 9a and b). Ant mounds also were numerous in the seawards advancing fore-dunes behind Kowhai Beach.
Fig. 9. Mean values of bee mound and ant mound abundance (+/− SE) within three habitats (hill, transition and sand)(a), with sand-cast fill of former kauri tree arrowed; and percent vegetation (shrubs, grass) and rock cover within the same three habitats at Kowhai Bay (b). Abundance of bee and ant burrows in the three identified habitats (c).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Fig. 10. Surface exposed in stepped sampling reveals three types of burrows; fresh and open (1), fresh and back filled (2), old and iron stained (3)(a); and graphical representation of mean abundance(+/−SE) of open holes at different depth intervals between 1–10 cm; note the concentration at a depth of 10 cm (b); each line = one burrow excavation series.
co-occurrence of gasteruptid wasps and colletid bees in early summer is consistent with their biological interactions. Those bee burrows that only extended to depths of 8–10 cm may have been intentional blind dead ends, or were abandoned during the course of bee excavation for one reason or another (e.g., unsuitable substrate, wasp predation, changing weather conditions, disturbance, etc). 5. Discussion The local, Aupouri Peninsula “coffee rock,” and dark brown or black, weakly consolidated, sub-Recent, sandy humic paleosols, host
109
occasional clavate burrows. These are typically filled with contrasting light-coloured fine sand described in a previous study (see Gregory et al., 2004, Fig. 8c), and bear resemblances to flask-shaped chambers that are often attributed to solitary bees (e.g. Hasiotis, 2003, Fig. 12G). However, features such as evidence of cell walls, antechambers, or capped spiral closures were never observed. Donovan (1983, p. 515) has noted that while New Zealand's clayey, silty and sandy soils are suitable for native bee nesting, vegetation may be so dense in places that access for the bees is difficult. Nevertheless, he has illustrated clustered native bee cells (Leioproctus fulvescens) nested in shallow soil burrows that revealed pollen, an egg and small larvae (Donovan, 1983, Fig. 1). Clusters of this kind were not recognized in the present study. Donovan has also further commented that heavy mineralized soils, such as those common in New Caledonia “…may render excavations by bees rather difficult” (Donovan, 1983, p. 515). Kowhai Bay “coffee rock” often exhibits limonite-rich horizons that are similarly hard and resistant. The vertical shafts, with depths reaching 1 m attained by some Leioproctus bees, and their burrowing/excavating rate of 4 cm/h in this type of lithology, is remarkable and surprising, as this would demand considerable energy expenditure. While some of the open vertical shafts terminated in a slightly enlarged ovoidal brood chamber (cell), many if not most did not. These simple, open shafts, some of which reach depths approaching a metre, are smoothwalled and if preserved could be considered Skolithos. This observation furthers the arguments (now becoming urgent) for a comprehensive review of Skolithos and its various ichnospecies, together with their value as environmental indicators (e.g., Gregory et al., 2006). The “Skolithos” shafts that have been exposed originate at deflation surfaces in “coffee rock”. There are substantial age differences between the local “coffee rock” basement lithology (? last glacial maxima; P. Augustinus, pers. com.), the discontinuous covering of Recent unconsolidated dune sands, and the activities of today's burrowing bees. The relationship can be likened to that recognized in bored (i.e., Gastrochaenolites) hard- and firm- or stiff-grounds, and omission surfaces in marine settings. Hence, the vertical bee shafts constitute an omission suite (sensu Bromley, 1975). We have yet to identify in the Quaternary paleosols and “coffee rock” sequences of Kowhai Beach, and nearby Henderson Bay and Cape Karikari, the array of insect-produced trace fossils that are widely reported from South America and elsewhere, and which define the recently recognized archetypal, non-marine, invertebrate Coprinisphaera ichnofacies (see Genise et al., 2000; Genise, 2004). However, many exposures of semi-consolidated, latest Holocene sand dunes, as well as older “coffee rock” in northern New Zealand host mottled fabrics that do not appear to have a particularly strong vertical component. It is tempting to suggest that this common fabric may be evidence for a locally depauperate Coprinisphaera ichnofacies,
Fig. 11. Remnant evidence for the once extensive forest (kauri) cover: a tree root with dark sandy humic halo infilled with white fine sand (a) and later invertebrate burrows through this substrate, back-filled with dark sand probably derived from hosting “coffee rock” (b) (width of scraper blade = 8 cm).
110
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
reflecting the depauperate, endemic nature of these insects in New Zealand. Chambered or clustered bee brooding cells (or combs) of the kind recognized by Genise and Bown (1996) (e.g. Rosellichnus and Uruguay) were never identified in the “coffee rocks” and paleosols of Kowhai Bay and nearby localities. Our observations suggest that the burrowing and over-printing activities of a solitary endemic bee (Leioproctus (Leioproctus) metallicus) have been a significant factor in the development of a pervasive mottled fabric that characterizes Pleistocene and Quaternary “coffee rock” and paleosol exposures of Kowhai Bay. It must also be appreciated that there may be substantial age differences between sediment deposition, subsequent indurated “coffee rock” development and insect burrowing (i.e., Skolithos creation). However, both ichnofabrics and pedofabrics in these “coffee rocks” and paleosols were overprinted in places by roots from the once extensive kauri forest cover (e.g. Fig. 11), and also may have significantly influenced groundwater movement through these iron-rich strata. Cloud et al.'s (1980) study of social insects as pseudofossils succinctly negates the once-touted age of the “oldest known metazoan”, and is a salutary lesson demonstrating that intimate association in space is not necessarily evidence for a strictly coeval relationship in time. 6. Conclusions In summary, the relevant aspects of this study are that: 1. Three distinctive native bee and ant habitats have been identified — “coffee rock” firmground exposures, rippled sand flats, and a vegetated transition zone in between. 2. Active solitary bee burrowing is largely restricted to consolidated “coffee rock” environments, with or without a thin, unconsolidated sand cover; ants are common to all three habitats. 3. Bee and ant tumuli are different in many aspects, with conical pelleted mounds indicative of the former, and low, crescentic, granular sandy mounds with a central depression typical of the latter. Subterranean burrows of each are also distinct, with bee burrows simple, deep and largely vertical (cf. Skolithos), and ant burrows dominantly dendritic, galleried, thin, mucus-lined, and extending horizontally. 4. The burrowing activities of Leioproctus sp. are driven by reproduction and concealment of larvae/larval food (pollen balls) from local cleptoparasitoid wasp predators. Burrowing rates of up to 4 cm/h can result in production of single shafts to 1 m depth, some terminating in small, bulbous chambers lined with secretions and, in places, containing larvae and/or stuffed with pollen. The uppermost 10 cm of many shafts are plugged with sand, likely hiding burrow openings from the gasteruptid wasps. 5. Consolidated dune sands throughout northernmost New Zealand are riddled with ubiquitous, iron-stained burrow mottling. Surface exposures of “coffee rock” are, in places, heavily pock-marked with bee borings comparable to Skolithos. These bare, modern-day surfaces can be considered the terrestrial equivalent of omission suites in marine environments and, in the case of Kowhai Bay, overprint the tree root-insect associations of a long-gone Kauri forest. Acknowledgements This study had funding support from the University of Auckland Research Committee (grants 9349/3602468 and /3421326). We are appreciative of Norman Wagener's permission to access the Kowhai site on several occasions. Thanks to Louise Cotterall for her patience and drafting skills, to Ewen Cameron for identification of Kunzea, and to Brian Donovan for assistance with bee identifications. We also acknowledge the careful attention given by an anonymous reviewer.
References Anonymous, 2002. Feathery Leioproctus bee fact file. http://faunanet.gov.au/wos/ factfile.cfm?Fact_ID=237. Batra, S.W., 1984. Solitary bees. Scientific American 250, 86–93. Bromley, R.G., 1975. Trace fossils at omission surfaces. In: Frey, R.W. (Ed.), The Study of Trace Fossils: a Synthesis of Principles, Problems and Procedures in Ichnology. Springer-Verlag, New York, pp. 399–428. Cloud, P., Gustafson, L.B., Watson, J.A.L., 1980. The works of living social insects as pseudofosils and the age of the oldest known metazoan. Science 210, 1013–1015. Don, W., 2007. Ants of New Zealand. Otago University Press, Dunedin. 240 pp. Donovan, B.J., 1980. Interactions between native and introduced bees in New Zealand. New Zealand Journal of Ecology 3, 104–116. Donovan, B.J., 1983. Comparative biogeography of native Apoidea of New Zealand and New Caledonia. GeoJournal 7, 511–516. Donovan, B.J., 1984. Native bees. In: Scott, R.R. (Ed.), New Zealand Pest and Beneficial Insects. Lincoln University College of Agriculture, pp. 247–251. Donovan, B.J., 2007. Fauna of New Zealand (Ko te Pepeke o Aotearoa): no 57. Apoidea (Insecta: Hymenoptera). Manaaki Whenua Press, New Zealand. Lincoln, Canterbury, 295 pp. Elliot, D.K., Nations, J.D., 1998. Bee burrows in the Late Cretaceous (Late Cenomanian) Dakota formation, northeastern Arizona. Ichnos 5, 243–253. Genise, J.F., 1979. Utilización de moldes de acrílico en el estudio de nidos de avispas cavadoras. Revista de la Sociedad Entomologica Argentina 38, 79–82. Genise, J.F., 2000. The ichnofamily Celliformidae for Celliforma and allied ichnogenera. Ichnos 7, 267–284. Genise, J.F., 2004. Ichnotaxonomy and ichnostratigraphy of chambered trace fossils in palaeosols attributed to coleopterans, ants and termites. In: McIlroy, D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis. Geological Society, London, Special Publications, vol. 228, pp. 419–453. Genise, J.F., Bown, T.M., 1996. Uruguay Roselli 1938 and Rosellichnus, n. ichnogenus: two ichnogenera for clusters of fossil bee cells. Ichnos 4, 199–217. Genise, J.F., Poiré, D.G., 2000. Fluidization in insect constructions in soils. Ichnos 7, 127–134. Genise, F.F., Mángano, M.G., Buatois, L.A., Laza, J.H., Verde, M., 2000. Insect trace fossils associations in paleosols: the Coprinisphaera Ichnofacies. Palaios 15, 49–64. Genise, J.F., Sciutto, J.C., Laza, J.H., Gonzalez, M.G., Bellosi, E.S., 2002. Fossil bee nests, coleopteran pupal chambers and tuffaceous paleosols from the Late Cretaceous Laguna Palacios Formation, Central Patagonia (Argentina). Palaeogeography, Palaeoclimatology, Palaeoecology 177, 215-235. Genise, J.F., Bellosi, E.S., Gonzalez, M.G., 2004. An approach to the description and interpretation of ichnofabrics in palaeosols. In: McIlroy, D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis. Geological Society, London, Special Publications, vol. 228, pp. 355–382. Gregory, M.R., Campbell, K.A., 2003. A ‘Phoebichnus look-alike’: a fossilized root system from Quaternary coastal dune sediments, New Zealand. Palaeogeography, Palaeoclimatology, Palaeoecolology 192, 147–258. Gregory, M.R., Martin, A.J., Campbell, K.A., 2004. Compound trace fossils formed by plant and animal interactions: Quaternary of northern New Zealand and Sapelo Island, Georgia (USA). Fossils and Strata 51, 88–103. Gregory, M.R., Campbell, K.A., Alfaro, A.C., Hudson, N., 2005. The bees' knees: burrows in consolidated Quaternary sands from Kowhai Bay, Northland, New Zealand. In: Campbell, K.A., Gregory, M.R. (Eds.), Programme and Abstracts, 8th International Ichnofabric Workshop, 17th-23rd February 2005. Auckland, New Zealand, pp. 40–41. Gregory, M.R., Campbell, K.A., Zuraida, R., Martin, A.J., 2006. Plant traces resembling Skolithos. Ichnos 13, 205–216. Hasiotis, S.T., 2003. Complex ichnofossils of solitary and social soil organisms: understanding their evolution and roles in terrestrial paleoecosystems. Palaeogeography, Palaeoclimatology, Palaeoecology 192, 259–320. Hicks, D.L., 1975. Geomorphic development of the southern Aupouri and Karikari Peninsulas, with special reference to sand dunes. Unpublished MA thesis, University of Auckland, 137 pp. Jennings, J.T., Austin, A.D., 2002. Systematics and distribution of world hyptiogastrine wasps (Hymenoptera:Gasteruptiidae). Invertebrate Systematics 16, 735–811. Mikuláš, R., 2001. Modern and fossil trace in terrestrial lithic substrates. Ichnos 8, 177–184. Mikuláš, R., Cilek, V., 1998. Terrestrial insect bioerosion and the possibilities of its fossilization (Holocene to Recent, Czech Republic). Ichnos 5, 325–333. Retallack, G.J., 1984. Trace fossils of burrowing beetles and bees in an Oligocene paleosol, Badlands National Park, South Dakota. Journal of Paleontology 58, 571–592. Roberts, E.M., Tapanila, L., 2006. A new social insect nest from the Upper Cretaceous Kaiparowits Formation of Southern Utah. Journal of Paleontology 80, 768–774. Stanley, K.O., Fagerstrom, J.A., 1974. Miocene invertebrate trace fossils from a braided river environment, western Nebraska, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 15, 63–82. Tschinkel, W.R., 2003. Subterranean ant nests: trace fossils past and future? Palaeogeography, Palaeoclimatology, Palaeoecology 192, 321–333. Waller, J.B., 1984. Household pests. In: Scott, R.R. (Ed.), New Zealand Pest and Beneficial Insects. Lincoln University College of Agriculture, pp. 205–206. Williams, D.F., Lofgren, C.S., 1988. Nest casting of some ground-dwelling Florida ant species using dental labstone. In: Brill, E.J. (Ed.), Advances in Myrmecology. Leiden, New York, pp. 433–443.
Contents lists available at ScienceDirect
Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Bee and ant burrows in Quaternary “coffee rock” and Holocene sand dunes, Kowhai Bay, Northland, New Zealand Murray R. Gregory a, Kathleen A. Campbell a,⁎, Andrea C. Alfaro b, Neville Hudson a a b
School of Geography, Geology and Environmental Science, The University of Auckland, Private Bag 92019, Auckand 1142, New Zealand School of Applied Sciences, Auckland University of Technology, Private Bag 92006, Auckland 1142, New Zealand
a r t i c l e
i n f o
Article history: Received 23 November 2007 Received in revised form 30 October 2008 Accepted 2 December 2008 Keywords: Bees and ants Surface mounds and burrows Quaternary “coffee rock” Palaeosols Northland New Zealand
a b s t r a c t Curious, multi-coloured, and pelleted sand mounds (tumuli) constructed by solitary bees, together with similar, but loosely piled white sand mounds made by ants, are a striking feature of deflation and erosion surfaces in coastal sand dune territory of northernmost New Zealand. These native bee and ant mounds (to N 20 mounds/m2) are found, respectively, on consolidated Quaternary “coffee rock” or atop shifting modern dune sands at Kowhai Bay, Aupouri Peninsula, across an area of several hundred square metres of bare and/or partly vegetated ground, lying some 800 m inland from the open ocean-facing Kowhai Beach. The vicinity is otherwise covered by scrubland vegetation dominated by the local ti tree, kanuka (Kunzea ericoides, var. linaris), and the aggressive introduced alien, Acacia longifolium, which bloom in spring or summer, respectively, attracting bees, ants and other insects to the area. Many of the pelleted bee mounds are connected to simple and open, vertical to steeply inclined cylindrical shafts (cf. Skolithos) that may reach depths approaching one metre. The shafts sometimes terminate in a slightly ovoidal chamber (cell) that is lined with translucent, mucoidal, parchment-like layers and/or stuffed with pollen, and which occasionally contains a single white larva. These biogenic structures are created by solitary endemic colletid bees (Leioproctus (Leioproctus) metallicus) which we observed burrowing vertically through firm “coffee rock” at rates of up to 4 cm/hour. Many of these shafts are plugged near the surface by sand (uppermost 10 cm), or dead-end at shallow depths, suggesting concealment and decoy strategies used to avoid the bees’ natural predator, parasitic gasteruptid wasps. In contrast to the pelleted and multi-coloured bee mounds, those made by ants (e.g., Monomorium antarcticum) are uniformly pale grey or white in colour, with a granular and smooth, fine to medium sand surface (i.e., they are non-pelleted). These ant mounds are crescent-shaped to circular, with a conspicuous central entrance hole that lies in a cratered depression, and which opens into irregularly branching burrows and passages that lack a lining other than some weak and discontinuous mucus-like coating (cf. Socialites). Quadrat sampling suggests that bee and ant mound distributions are oppositely related to substrate coherency. Field excavations indicate strong overprinting by bee excavations on consolidated dune fabrics. It is suggested that their burrows may have influenced groundwater movement in these iron-rich, paleosolbearing strata. They also imply a paleoenvironmental shift from Kauri forest cover to deflationary sand dune episodes in the semi-tropical climate of the late Quaternary of northern New Zealand. The terrestrial deflationary setting can be likened to omission surfaces of marine environments. © 2008 Elsevier B.V. All rights reserved.
1. Introduction: endemic bees and ants of Kowhai Bay, New Zealand Both bees and ants are elements of the depauperate New Zealand insect biota, and their taxonomy has only recently been the subject of thorough and detailed investigation (e.g., Donovan, 2007, bees; and Don, 2007, ants). There are at least 40 species of bees endemic to New Zealand, with all of them belonging to the two most primitive bee families — Colletidae and Halictidae. Of these, 36 are representatives ⁎ Corresponding author. Tel.: +64 9 373 7599; fax: +64 9 373 7435. E-mail address: [email protected] (K.A. Campbell). 0031-0182/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2008.12.008
of the former. The native New Zealand bee biota, and also that of New Caledonia 1600 km to the NNW with 28 species, are depauperate when compared with their continental Australian source where N950 species have been identified (Donovan, 1980, 1983). Typical local nesting sites for bees of the colletid family are areas of barren or semibare ground that are free from excess moisture over the late springsummer nesting season. Nests typically consist of simple tunnels or burrows which extend to depths of 20–50 cm and commonly terminate in pollen-stuffed, ovoidal cavities (brood cells) (Donovan, 1980, 1983, 1984, 2007). They feed on, and gather pollen from, local flowering plants, but in New Zealand are particularly attracted to ti trees, manuka and kanuka (Leptospermum scorparium and Kunzea
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
ericoides var. linaris), which are dominant features of the flora of northern New Zealand scrublands. Of some 37 established ant species recognized in New Zealand, 10 or 11 are generally accepted to be endemic and most of the remainder are considered recent arrivals from Australia (Waller, 1984; Don, 2007). While bee mounds (tumuli) are restricted to areas of consolidated Quaternary “coffee rock”, they share these exposed surfaces with ant mounds. The ant mounds also are persistent across broad, shifting sand-flat areas and can be followed into sand beaches for a short distance above high tide level. Excavations into loose sands and “coffee rock” generally expose galleried passages, some of which
103
can be traced laterally for distances of 2 m or more and may reach depths exceeding 70 cm. The primary objectives of this study were to further our understanding of the role played by the burrowing activities of local bees and ants in the Quaternary “coffee rock” of Kowhai Bay, and their significance in the resulting development of overprinted ichno- or pedofabrics. 2. Setting: Kowhai Bay Over Quaternary times, northwards drifting sands fed the growth of two large tombolos in the region. These have permanently linked to
Fig. 1. Kowhai Bay with sampling locality indicated by “x”; 20 m contour defines extent of ridge crest.
104
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Fig. 2. General view looking eastwards along the arcuate length of Kowhai Bay. Note the build up of a substantial sandy foredune along its length, the irregular exposures of deflationary “coffee rock” surfaces (in foreground) and vegetation cover of 20 m ridge in middle-distance.
the mainland an archipelago of once upstanding, erosion resistant islands. Aspects of the Quaternary dunes and associated “coffee rock” paleoenvironments have been described in detail elsewhere (see Gregory and Campbell 2003; Gregory et al., 2004, 2005, 2006). Kowhai Bay is a minor arcuate indention, some 2 km in length, located towards the southern end of Aupouri Peninsula (Fig. 1). It faces northeastwards into Great Exhibition Bay and is protected to the north and south by prominent basement headlands Fig. 1. The land immediately behind
Kowhai Beach, and between it and Houhora Harbour (Fig. 1), rises abruptly to a conspicuous N20 m high ridge, typified by discontinuous, deflation exposures of consolidated “coffee rock” (i.e. compacted and weakly cemented strata dominated by humates and iron oxides) and case-hardened, limonitic crusts representing older, semi-indurated sand dunes (e.g. Hicks, 1975). The exposed surfaces are intermittently covered by present-day, wind blown, white to off white, drifting fine to medium sand (Fig. 2).
Fig. 3. Numerous and varied casting mounds in drifting sand on westerly facing, irregular surface and towards 20 m ridge crest; with deflationary surfaces arrowed (a); closer view with both bee (1) and ant (2) burrow mounds indicated (b); typical bee casting mound with pelleted surface and no entrance hole evident (c); “bulls eye” pattern of changing colours that reflects a bee's sequential passage though horizons of differing colour and the local “coffee rock” stratigraphy (d) (coin diam. = 21 mm).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
3. Mound and burrow characteristics 3.1. Bee mounds — general overview The study site covers an area of several thousand square metres, and lies some 800 m inland from the easterly facing, open-ocean shoreline. Here bare, irregular and undulating deflationary surfaces, cut across consolidated older Quaternary sands (“coffee rock”). A thin and patchy cover of contemporary drifting sand, irregularly interspersed with sand mounds is a noteworthy feature of this area and is particularly conspicuous across the crest and northwest flank of a low hill (Fig. 3a). During our spring visits (November–December), the air was buzzing with activities of a local colletid native bee (Leioproctus (Leioproctus) metallicus), and an endemic, cleptoparasitoid gasteruptid wasp (Pseudofoenus crassipes; female). On three occasions in the late spring and early summers of 2002, 2003 and 2004, this surface was covered with numerous mono- and multi-hued “casting” mounds (tumuli) (Fig. 3b–d). These conical structures were generally circular, 8–10+ cm diameter in outline and 2–N3 cm in height. At, or closely near each mound's central peak, there was commonly an open “entrance” hole, 0.5–1 cm across. In many instances the mounds were
105
built of elongate rod-like “pellets” (maximum length ~ 1 cm, diameter 3–4 mm), distributed in a crudely sub-radial pattern about their centre (Fig. 3d). Typically, in the sediment pile of these mounds, there was a veritable ‘rainbow’ display — a ‘bulls eye’ effect — with concentric colour changes (white, yellow, orange, brown, dark brown, purple, dark red, and charcoal). This pattern is a reflection of the different coloured sediment horizons being encountered by each tracemaker during excavation through varying depths (to N90 cm) (Fig. 3c and d). In others, the mounds were structureless with loose sand cascading from the central peak. The former were attributed to bee burrowing activities and are readily distinguished from the latter, which were made by ant activity across the same general area (see later sections). 3.2. Bee burrows — description and construction Where there was no drifting sand cover, exposed “coffee rock” surfaces were commonly pock-marked by sharply defined, circular, smooth-walled holes, ~ 1 cm in diameter, and which extended vertically to depths reaching 10 cm. These burrows did not branch and were otherwise blind. Shallow scraping through numerous
Fig. 4. After removal of surface-drifting, loose sand cover and scraping up to 10 cm in to the buried “coffee rock”, the open circular shafts (black) made by the bee Leioproctus (? Skolithos) come into view. Fresh-filled shafts (see large arrow) and old, iron stained plugged holes (see thin arrows) are also present (coin diam. = 30 mm) (a). Schematic diagram, illustrating mound and vertical access, plugged sloping segment, and vertical shaft with ovoidal brooding chamber (b).
106
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
mounds, and removal of drifting sand cover, exposed the surface of underlying “coffee rock”. Continued scraping and gradual removal of a layer 10–12 cm thick over an area of 0.75 m2 commonly revealed a number of once “hidden”, open and vertical to steeply inclined circular shafts 8–10 mm in diameter (Fig. 4a). The upper parts of these shafts had been plugged by sand over a depth of 5–10 cm or more (Fig. 4b). Excavation and probing in the “coffee rock” have shown that some of the simple open shafts extend (more or less vertically) to depths of at least 95 cm with no intervening obstructions and bear remarkable resemblance to the ichnogenus Skolithos. Comparable bee burrowing activities are a widely reported activity in palaeosols (e.g., Stanley and Fagerstrom, 1974; Retallack, 1984; Elliot and Nations, 1998; Mikuláš and Cilek, 1998; Genise et al., 2004) and exposures of castellated sandstones (e.g., Mikuláš, 2001). Bee burrowing and shaft excavation is a seasonal activity — late spring to early summer (mid November to early January), and over the period when ti tree (manuka and kanuka) was in full bloom. After a seemingly random, if not irrational and irregular search, while flying over and sometimes landing briefly across an area of a square metre or so, bees settle on “selected appropriate” sites. There they build mounds by “cork-screwing” their way into and through a shallow layer of loose, surface-drifting soft sand. In so doing they quickly disappear from view (Fig. 5a–d). At a depth of a few centimetres they are commonly excavating into a consolidated and firm “coffee rock” substrate. Observations were made of L. metallicus bees released into a glass terrarium packed with Kowhai Beach-sourced, loose and
weakly compacted, dampened sand. These observations showed that this sediment substrate was being manipulated between the bees’ abdomen and legs and quickly “kneaded” into rod-like pellets. These pellets were pushed progressively upwards to emerge in or left exposed at the sandy sediment surface. Individual bees continued to bring forth material from depth without themselves necessarily reappearing at the surface (Fig. 5b). The process must involve liquefaction and/or fluidization similar to that described by Genise and Poiré (2000). Sequential, field observations on one day, over a period of several hours, suggest the bee-burrowing rate may reach 4 cm/h. At this rate, burrowing to a depth of 90 cm could take N24 h! Temperatures measured at the base of deep burrow shafts were 2–3 °C cooler than those of the sun-drenched surface above, and the substrate was slightly moist at depth as well. By the end of early summer (January), both adult colletid bees and the cleptoparasitoid gasteruptid wasps had mostly disappeared (see also Section 4). The bee mounds had also vanished, for these quickly disintegrate with wind and rain. In the following months (February–June) Acacia came into flower and introduced honey-bees (Apis mellifera) became numerous. Hence, the honey bee/Acacia association is temporally exclusive to the colletid bee/ti tree association in the same locale. 3.3. Brood cells Several deep vertical shafts of the bee burrows terminated at their base in a solitary, slightly expanded and ovoidal chamber. These
Fig. 5. Sequence of bee moving around and corkscrewing its way into the sand substrate before disappearing from view (a–d) and pushing a pellet to the surface without emerging (e); early mound development after three or four hours activity (f); live bee in glass terrarium, actively kneading a sandy pellet (dashed) and which was moved subsequently towards the surface (g).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
107
“brood cells” were sometimes lined with a thick and somewhat brittle, cellophane-like secretion, that probably hardens after being applied by the female's tongue (Anonymous, 2002), and also helps to keep the chamber dry from external moisture (Batra, 1984). Lower parts of some shafts were similarly lined, and slugs or pellets of pollen were occasionally encountered at the base of excavated shafts. In rare instances a solitary larval inhabitant was present (Fig. 6a–b). Short simple and rarely branching, lateral tunnels coming off open vertical shafts were uncommon and generally blind. These were never observed to open into multiple brooding cells set in sophisticated and whorled or tiered patterns of the kind associated with the ichnofamily Celliformidae. Nonetheless, Celliformidae also includes ichnogenera of simple morphology like Celliforma itself, and Palmiraichnus (e.g. Elliot and Nations, 1998, Figs. 5 and 6; Genise, 2000, Figs. 1 and 2; Genise et al., 2002, Fig. 6; Hasiotis, 2003, Fig. 3). In rare instances the termination of these short tunnels was slightly expanded and could host a pollen slug or a solitary white larva. 3.4. Ant mounds When fresh, mounds made by a local endemic ant (Monomorium antarcticum) in the same area are easily distinguished from those made by native bees. They are smooth surfaced, typically built of loosely packed, pale cream-coloured or white, surface drifting medium to fine sand, and tumuli slopes were never pelleted. These mounds typically exhibited a crudely “half-moon” crescent shape in plan view, volcanolike in cross-section, and tended to be slightly broader than bee casting mounds (Fig. 7a and b, 8a). Ant mounds typically had a central, or slightly off-set entrance hole that lay in shallow depressions that were
Fig. 7. Typical ant mounds from sand flat habitats; note the absence of pelleted surfaces and limited evidence for excavations into “coffee rock”(a, b); entrance holes are often conspicuously off-set (a) and crescentic in shape, with the mound surface sloping away from the entrance — a volcano in miniature that is beached on one side (b) (coin diam. = 30 mm).
often breached to one side. Ant tunnels are generally much smaller than bee shafts (1 mm to b10 mm). Although the diameter of some major passages may exceed 1 cm, they are often highly irregular and roughly surfaced (Fig. 8b). Very small, irregularly distributed, and generally difficult to identify entrances (unless ants are coming and going) may be present across mound surfaces. Adopting procedures developed by several earlier authors (e.g., Genise, 1979; Williams and Lofgren, 1988; Tschinkel, 2003), a number of casts have been made with an orthodontal plaster slurry (labrock or labstone). An example is illustrated in Fig. 8c. Ant colonies may have numerous minor entranceways common to a major tunnel, which leads to a complex of open irregular passages and pillared-galleries that are stacked at intervals to depths of N60 cm. These are neither as well developed nor as systematically organized as those illustrated by Tschinkel (2003, e.g., Figs. 5 and 9). Crude nesting patterns revealed during excavations (Fig. 8b) bear similarities to the ichnospecies Socialites tumulus recently described by Roberts and Tapanila (2006), and attributed by them to ant activity. Some of the major tunnels or burrows are discontinuously interconnected by finer tubular passages and have lateral sloping and/or horizontal extents of two metres or more (Fig. 8c). 4. Distribution of bee and ant burrows at Kowhai Bay Three distinctive habitats were identified across the study area. Their distribution patterns are illustrated in Fig. 9a–c. Fig. 6. Parchment-like surface lining of brood cell (a), empty pupal cell (large arrow) lying alongside its removed larval inhabitant (thin arrow, b).
1:- On the flanks and towards the ridge-crest of older and consolidated “coffee rock” exposures, the habitat was largely bare
108
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Towards the ridge crest, where most of the bee burrows were observed, 12 1-m2 quadrats were excavated to 45 cm, exposing a number of open shafts, a few of which could be traced continuously through the vertical depth of an excavation. The number of open holes (Fig. 4a), freshly sand-filled holes (defined by sharp boundaries), and old (iron stained, diffuse boundaries) filled burrows were recorded at set depth intervals (0–5, 6–14, 15–24, 25–35, 36–46 cm) during the excavations (Fig. 9a and b). The overall trend is for all burrow types to decrease in number with increasing depth. At depth, old filled burrows were about six times more abundant than the other two types. In addition, a peak in open holes was identified at approximately 10 cm below the surface in the majority of quadrats (Fig. 10). Fewer open holes at the surface, compared to those at a depth of 10 cm, may be explained by the bees’ behaviour of plugging the tops of holes through depths 0–10 cm, with the objective of concealing them from predators, such as cleptoparasitic (predatory-inquiline) gasteruptid wasps. Pseudofoenus is known to be a predator-inquiline on colletid bees (Jennings and Austin, 2002), and hence the female lays its egg upon the larva of the bee such that the emergent wasp larva consumes the pollen ball and/or the bee larva within the burrow of the bee. Thus, the temporal
Fig. 8. A shallow vertical excavation reveals white, sand-filled, irregular galleries at shallow depth beneath a “volcanic” ant mound (arrowed) (a) (pen-knife = 9 cm) and fresh, currently active and open burrows at greater depth (coin diam. = 21 mm). Other excavations have exposed substantial and open sub-horizontal galleries of varying size (b) and with numerous small vertical access paths/burrows, many of which can be traced into surface “volcano-shaped mounds”. Some of the large galleries have been traced for distances reaching N2 m. Casts were made with “labrock plaster,” introduced as a thin slurry poured into major surface entrance holes (c).
ground with a few patches of drifting sand and widely spaced scrubby plants. 2:- Distally from the ridge crest, a rippled sand flat is dominated by soft sandy substrates with minor patches of grass. 3:- Between these two habitats lies a transition zone with varying mixtures of shrub-covered ground, grassy areas and sand. Bee burrows were most abundant in extensive patches of bare ground towards the ridge crest, they were rare in the transition zone, and absent from the soft sand flat habitat, as well as missing from the open ocean-facing back beach and sandy fore-dunes. Ant mounds were present and conspicuous in all three habitats, with abundance increasing from the ridge crest (i.e., “hill” in Fig. 9) towards the sand flats (Fig. 9a and b). Ant mounds also were numerous in the seawards advancing fore-dunes behind Kowhai Beach.
Fig. 9. Mean values of bee mound and ant mound abundance (+/− SE) within three habitats (hill, transition and sand)(a), with sand-cast fill of former kauri tree arrowed; and percent vegetation (shrubs, grass) and rock cover within the same three habitats at Kowhai Bay (b). Abundance of bee and ant burrows in the three identified habitats (c).
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
Fig. 10. Surface exposed in stepped sampling reveals three types of burrows; fresh and open (1), fresh and back filled (2), old and iron stained (3)(a); and graphical representation of mean abundance(+/−SE) of open holes at different depth intervals between 1–10 cm; note the concentration at a depth of 10 cm (b); each line = one burrow excavation series.
co-occurrence of gasteruptid wasps and colletid bees in early summer is consistent with their biological interactions. Those bee burrows that only extended to depths of 8–10 cm may have been intentional blind dead ends, or were abandoned during the course of bee excavation for one reason or another (e.g., unsuitable substrate, wasp predation, changing weather conditions, disturbance, etc). 5. Discussion The local, Aupouri Peninsula “coffee rock,” and dark brown or black, weakly consolidated, sub-Recent, sandy humic paleosols, host
109
occasional clavate burrows. These are typically filled with contrasting light-coloured fine sand described in a previous study (see Gregory et al., 2004, Fig. 8c), and bear resemblances to flask-shaped chambers that are often attributed to solitary bees (e.g. Hasiotis, 2003, Fig. 12G). However, features such as evidence of cell walls, antechambers, or capped spiral closures were never observed. Donovan (1983, p. 515) has noted that while New Zealand's clayey, silty and sandy soils are suitable for native bee nesting, vegetation may be so dense in places that access for the bees is difficult. Nevertheless, he has illustrated clustered native bee cells (Leioproctus fulvescens) nested in shallow soil burrows that revealed pollen, an egg and small larvae (Donovan, 1983, Fig. 1). Clusters of this kind were not recognized in the present study. Donovan has also further commented that heavy mineralized soils, such as those common in New Caledonia “…may render excavations by bees rather difficult” (Donovan, 1983, p. 515). Kowhai Bay “coffee rock” often exhibits limonite-rich horizons that are similarly hard and resistant. The vertical shafts, with depths reaching 1 m attained by some Leioproctus bees, and their burrowing/excavating rate of 4 cm/h in this type of lithology, is remarkable and surprising, as this would demand considerable energy expenditure. While some of the open vertical shafts terminated in a slightly enlarged ovoidal brood chamber (cell), many if not most did not. These simple, open shafts, some of which reach depths approaching a metre, are smoothwalled and if preserved could be considered Skolithos. This observation furthers the arguments (now becoming urgent) for a comprehensive review of Skolithos and its various ichnospecies, together with their value as environmental indicators (e.g., Gregory et al., 2006). The “Skolithos” shafts that have been exposed originate at deflation surfaces in “coffee rock”. There are substantial age differences between the local “coffee rock” basement lithology (? last glacial maxima; P. Augustinus, pers. com.), the discontinuous covering of Recent unconsolidated dune sands, and the activities of today's burrowing bees. The relationship can be likened to that recognized in bored (i.e., Gastrochaenolites) hard- and firm- or stiff-grounds, and omission surfaces in marine settings. Hence, the vertical bee shafts constitute an omission suite (sensu Bromley, 1975). We have yet to identify in the Quaternary paleosols and “coffee rock” sequences of Kowhai Beach, and nearby Henderson Bay and Cape Karikari, the array of insect-produced trace fossils that are widely reported from South America and elsewhere, and which define the recently recognized archetypal, non-marine, invertebrate Coprinisphaera ichnofacies (see Genise et al., 2000; Genise, 2004). However, many exposures of semi-consolidated, latest Holocene sand dunes, as well as older “coffee rock” in northern New Zealand host mottled fabrics that do not appear to have a particularly strong vertical component. It is tempting to suggest that this common fabric may be evidence for a locally depauperate Coprinisphaera ichnofacies,
Fig. 11. Remnant evidence for the once extensive forest (kauri) cover: a tree root with dark sandy humic halo infilled with white fine sand (a) and later invertebrate burrows through this substrate, back-filled with dark sand probably derived from hosting “coffee rock” (b) (width of scraper blade = 8 cm).
110
M.R. Gregory et al. / Palaeogeography, Palaeoclimatology, Palaeoecology 273 (2009) 102–110
reflecting the depauperate, endemic nature of these insects in New Zealand. Chambered or clustered bee brooding cells (or combs) of the kind recognized by Genise and Bown (1996) (e.g. Rosellichnus and Uruguay) were never identified in the “coffee rocks” and paleosols of Kowhai Bay and nearby localities. Our observations suggest that the burrowing and over-printing activities of a solitary endemic bee (Leioproctus (Leioproctus) metallicus) have been a significant factor in the development of a pervasive mottled fabric that characterizes Pleistocene and Quaternary “coffee rock” and paleosol exposures of Kowhai Bay. It must also be appreciated that there may be substantial age differences between sediment deposition, subsequent indurated “coffee rock” development and insect burrowing (i.e., Skolithos creation). However, both ichnofabrics and pedofabrics in these “coffee rocks” and paleosols were overprinted in places by roots from the once extensive kauri forest cover (e.g. Fig. 11), and also may have significantly influenced groundwater movement through these iron-rich strata. Cloud et al.'s (1980) study of social insects as pseudofossils succinctly negates the once-touted age of the “oldest known metazoan”, and is a salutary lesson demonstrating that intimate association in space is not necessarily evidence for a strictly coeval relationship in time. 6. Conclusions In summary, the relevant aspects of this study are that: 1. Three distinctive native bee and ant habitats have been identified — “coffee rock” firmground exposures, rippled sand flats, and a vegetated transition zone in between. 2. Active solitary bee burrowing is largely restricted to consolidated “coffee rock” environments, with or without a thin, unconsolidated sand cover; ants are common to all three habitats. 3. Bee and ant tumuli are different in many aspects, with conical pelleted mounds indicative of the former, and low, crescentic, granular sandy mounds with a central depression typical of the latter. Subterranean burrows of each are also distinct, with bee burrows simple, deep and largely vertical (cf. Skolithos), and ant burrows dominantly dendritic, galleried, thin, mucus-lined, and extending horizontally. 4. The burrowing activities of Leioproctus sp. are driven by reproduction and concealment of larvae/larval food (pollen balls) from local cleptoparasitoid wasp predators. Burrowing rates of up to 4 cm/h can result in production of single shafts to 1 m depth, some terminating in small, bulbous chambers lined with secretions and, in places, containing larvae and/or stuffed with pollen. The uppermost 10 cm of many shafts are plugged with sand, likely hiding burrow openings from the gasteruptid wasps. 5. Consolidated dune sands throughout northernmost New Zealand are riddled with ubiquitous, iron-stained burrow mottling. Surface exposures of “coffee rock” are, in places, heavily pock-marked with bee borings comparable to Skolithos. These bare, modern-day surfaces can be considered the terrestrial equivalent of omission suites in marine environments and, in the case of Kowhai Bay, overprint the tree root-insect associations of a long-gone Kauri forest. Acknowledgements This study had funding support from the University of Auckland Research Committee (grants 9349/3602468 and /3421326). We are appreciative of Norman Wagener's permission to access the Kowhai site on several occasions. Thanks to Louise Cotterall for her patience and drafting skills, to Ewen Cameron for identification of Kunzea, and to Brian Donovan for assistance with bee identifications. We also acknowledge the careful attention given by an anonymous reviewer.
References Anonymous, 2002. Feathery Leioproctus bee fact file. http://faunanet.gov.au/wos/ factfile.cfm?Fact_ID=237. Batra, S.W., 1984. Solitary bees. Scientific American 250, 86–93. Bromley, R.G., 1975. Trace fossils at omission surfaces. In: Frey, R.W. (Ed.), The Study of Trace Fossils: a Synthesis of Principles, Problems and Procedures in Ichnology. Springer-Verlag, New York, pp. 399–428. Cloud, P., Gustafson, L.B., Watson, J.A.L., 1980. The works of living social insects as pseudofosils and the age of the oldest known metazoan. Science 210, 1013–1015. Don, W., 2007. Ants of New Zealand. Otago University Press, Dunedin. 240 pp. Donovan, B.J., 1980. Interactions between native and introduced bees in New Zealand. New Zealand Journal of Ecology 3, 104–116. Donovan, B.J., 1983. Comparative biogeography of native Apoidea of New Zealand and New Caledonia. GeoJournal 7, 511–516. Donovan, B.J., 1984. Native bees. In: Scott, R.R. (Ed.), New Zealand Pest and Beneficial Insects. Lincoln University College of Agriculture, pp. 247–251. Donovan, B.J., 2007. Fauna of New Zealand (Ko te Pepeke o Aotearoa): no 57. Apoidea (Insecta: Hymenoptera). Manaaki Whenua Press, New Zealand. Lincoln, Canterbury, 295 pp. Elliot, D.K., Nations, J.D., 1998. Bee burrows in the Late Cretaceous (Late Cenomanian) Dakota formation, northeastern Arizona. Ichnos 5, 243–253. Genise, J.F., 1979. Utilización de moldes de acrílico en el estudio de nidos de avispas cavadoras. Revista de la Sociedad Entomologica Argentina 38, 79–82. Genise, J.F., 2000. The ichnofamily Celliformidae for Celliforma and allied ichnogenera. Ichnos 7, 267–284. Genise, J.F., 2004. Ichnotaxonomy and ichnostratigraphy of chambered trace fossils in palaeosols attributed to coleopterans, ants and termites. In: McIlroy, D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis. Geological Society, London, Special Publications, vol. 228, pp. 419–453. Genise, J.F., Bown, T.M., 1996. Uruguay Roselli 1938 and Rosellichnus, n. ichnogenus: two ichnogenera for clusters of fossil bee cells. Ichnos 4, 199–217. Genise, J.F., Poiré, D.G., 2000. Fluidization in insect constructions in soils. Ichnos 7, 127–134. Genise, F.F., Mángano, M.G., Buatois, L.A., Laza, J.H., Verde, M., 2000. Insect trace fossils associations in paleosols: the Coprinisphaera Ichnofacies. Palaios 15, 49–64. Genise, J.F., Sciutto, J.C., Laza, J.H., Gonzalez, M.G., Bellosi, E.S., 2002. Fossil bee nests, coleopteran pupal chambers and tuffaceous paleosols from the Late Cretaceous Laguna Palacios Formation, Central Patagonia (Argentina). Palaeogeography, Palaeoclimatology, Palaeoecology 177, 215-235. Genise, J.F., Bellosi, E.S., Gonzalez, M.G., 2004. An approach to the description and interpretation of ichnofabrics in palaeosols. In: McIlroy, D. (Ed.), The Application of Ichnology to Palaeoenvironmental and Stratigraphic Analysis. Geological Society, London, Special Publications, vol. 228, pp. 355–382. Gregory, M.R., Campbell, K.A., 2003. A ‘Phoebichnus look-alike’: a fossilized root system from Quaternary coastal dune sediments, New Zealand. Palaeogeography, Palaeoclimatology, Palaeoecolology 192, 147–258. Gregory, M.R., Martin, A.J., Campbell, K.A., 2004. Compound trace fossils formed by plant and animal interactions: Quaternary of northern New Zealand and Sapelo Island, Georgia (USA). Fossils and Strata 51, 88–103. Gregory, M.R., Campbell, K.A., Alfaro, A.C., Hudson, N., 2005. The bees' knees: burrows in consolidated Quaternary sands from Kowhai Bay, Northland, New Zealand. In: Campbell, K.A., Gregory, M.R. (Eds.), Programme and Abstracts, 8th International Ichnofabric Workshop, 17th-23rd February 2005. Auckland, New Zealand, pp. 40–41. Gregory, M.R., Campbell, K.A., Zuraida, R., Martin, A.J., 2006. Plant traces resembling Skolithos. Ichnos 13, 205–216. Hasiotis, S.T., 2003. Complex ichnofossils of solitary and social soil organisms: understanding their evolution and roles in terrestrial paleoecosystems. Palaeogeography, Palaeoclimatology, Palaeoecology 192, 259–320. Hicks, D.L., 1975. Geomorphic development of the southern Aupouri and Karikari Peninsulas, with special reference to sand dunes. Unpublished MA thesis, University of Auckland, 137 pp. Jennings, J.T., Austin, A.D., 2002. Systematics and distribution of world hyptiogastrine wasps (Hymenoptera:Gasteruptiidae). Invertebrate Systematics 16, 735–811. Mikuláš, R., 2001. Modern and fossil trace in terrestrial lithic substrates. Ichnos 8, 177–184. Mikuláš, R., Cilek, V., 1998. Terrestrial insect bioerosion and the possibilities of its fossilization (Holocene to Recent, Czech Republic). Ichnos 5, 325–333. Retallack, G.J., 1984. Trace fossils of burrowing beetles and bees in an Oligocene paleosol, Badlands National Park, South Dakota. Journal of Paleontology 58, 571–592. Roberts, E.M., Tapanila, L., 2006. A new social insect nest from the Upper Cretaceous Kaiparowits Formation of Southern Utah. Journal of Paleontology 80, 768–774. Stanley, K.O., Fagerstrom, J.A., 1974. Miocene invertebrate trace fossils from a braided river environment, western Nebraska, USA. Palaeogeography, Palaeoclimatology, Palaeoecology 15, 63–82. Tschinkel, W.R., 2003. Subterranean ant nests: trace fossils past and future? Palaeogeography, Palaeoclimatology, Palaeoecology 192, 321–333. Waller, J.B., 1984. Household pests. In: Scott, R.R. (Ed.), New Zealand Pest and Beneficial Insects. Lincoln University College of Agriculture, pp. 205–206. Williams, D.F., Lofgren, C.S., 1988. Nest casting of some ground-dwelling Florida ant species using dental labstone. In: Brill, E.J. (Ed.), Advances in Myrmecology. Leiden, New York, pp. 433–443.