New records of springtails in New Zealand pasture: how well are our pastoral invertebrates known?

Abstract

Twenty-four collembolan species are recorded from improved pastures and clovers in New Zealand, of which 17 can be named to species or probable species, the others only to genus. Of the 17 named species, nine have been recorded before from New Zealand but the other eight are new records for the country. All named species are considered as introduced to New Zealand, probably originally from Europe and are unlikely to colonise native habitats. As all named species reported as new records can be abundant at times, this indicates poor knowledge of a major part of New Zealand's agricultural fauna. Collembola are a group of important microarthropod detritivores that make a significant contribution to ecosystem services. The absence so far of quantification of the contribution this and other soil groups make to ecological resilience and function is a serious problem.

Keywords:

• sustainable agriculture
• Collembola
• Brachystomellidae
• Hypogastruridae
• Orchesellinae

Introduction

Biodiversity is declining worldwide at the fastest rate since the last ice age (15,000 years ago). With that decline, invertebrate food webs are becoming simplified, largely as a result of agricultural expansion and intensification (Tylianakis et al. 2007). As a consequence, ecosystem services are declining, as are their economic values (Sandhu et al. 2012; Porter et al. 2009). Such services include soil formation and nutrient mineralisation and Collembola play an important role in all these processes (Schwartz et al. 2000).

In New Zealand, pastoral agriculture dominates the lowland landscape, with increasingly high inputs of fossil-fuel derived fertilisers (Sandhu et al. 2012). The variable and external costs associated with this practice are well known (Wratten et al. 2012), but little recognition is being given to the role of native and non-native fauna and their contribution to agricultural sustainability. This paper documents recent first records of eight abundant Collembola species in New Zealand pastures and asks whether ignorance of New Zealand's soil fauna is widespread and whether there is general ignorance of its contribution to maintaining current highly productive agriculture in pastoral and other sectors.

Methods

The new species records are derived from four collections taken from pasture over the last 20 years; three came from clover and improved pasture plots on agricultural land at Lincoln University, Canterbury, New Zealand, being used for agronomy trials. They were collected in 1994, 2010 and 2011. The fourth sample came from pasture at an experimental farm at Ballantrae, North Island, New Zealand (Table 1).

Table 1 . Collembolan species collected from improved pastures and lucerne crops in New Zealand. Brackets denote that it may have been recorded under a different name by Adams (1971).

Taxon		Previously recorded in Greenslade (2011)	Collection
Family	Genus/species		Ballantrae 1994 (Springett collection)	Lincoln University 1994 (Wratten collection)	Lincoln University 2010, 2011 (Wratten collection)	Lincoln University 2011 (McNeill collection)
Brachystomellidae	Brachystomella platensis Najt & Massoud, 1974	(No)	+		+
Neanuridae	Friesea spp	Unknown	+
Hypogasturidae	Ceratophysella denticulata (Bagnall, 1941)	Yes	+
	Hypogastrura vernalis (Carl, 1901)	No	Possible	+	+
	Hypogastrura manubrialis (Tullberg, 1869)	Yes				+
Tullbergiidae	Mesaphorura macrochaeta Rusek, 1976	(No)	+
Onychiuridae	Protaphorura cf. fimata (Gisin, 1952)	(No)	+
Isotomidae	Parisotoma spp	Unknown	+	+
	Hemisotoma thermophila (Axelson, 1900) gp	Yes (as Isotomina thermophila)	+
	Mucrosomia caeca (Wahlgren, 1906)	Yes (as Cryptopygus caecus)	+
	Isotomiella sp.	Unknown
	Isotomurus maculatus (Schäffer, 1896)	No				+
	Folsomides parvulus Stach, 1922	No	+
Tomoceridae	Heteromurus major (Moniez, 1889)	No	+	+ (Probable)	+
Entomobryidae	Entomobrya spp
	Sinella sp.	Unknown	+
	Pseudosinella sp.	Unknown	+
	Orchesellinae indet.	Unknown	+
Sminthurididae	Sphaeridia sp.	Unknown	+
Bourletiellidae	Bourletiella hortensis (Fitch, 1863)	Yes				+
	Bourletiella viridescens Stach, 1920	No			+
	Deuterosminthurus cf. sulphureus (Koch, 1840)	Yes	+
Sminthuridae	Sminthurus viridis (Linnaeus, 1758)	Yes			+	+

The Wratten 2010 and 2011 samples came from a long-term (16 years) field experiment at Lincoln University comparing different grassland managements. The site is located at 43°64′S and 172°47′E. A petrol-driven suction sampler was used, consisting of a modified leaf blower (MacLeod et al. 1994). The sampler, with a 0.02 m² sampling area, was run at full throttle against the pasture for 5 s. This was carried out 10 times in an experimental pasture treatment comprising four or five plant species, depending on the replicate, dominated by perennial ryegrass (Lolium perenne L.) and low-growing rosette-forming species such (Taraxacum officinale Weber) and Cat's Ear (Hypocharis radicata L.). The selected treatment was ‘irregularly mown’, this being defined as 2–5 times per year, with cutting triggered by the ryegrass reaching 30 cm in height. Clippings were returned to the plot on each mowing date. Collembola numbers were estimated by tipping the invertebrates while still alive into white plastic trays at the field site. Sub-samples of these insects were taken and stored in 75% ethyl alcohol.

The 2011 collection came from the Lincoln University Research Dairy farm (43°64′S, 172°46′E) using pitfall traps as well as suction (blower-vac) samples. Collection dates were 26 November 2010 and 4 March 2011. The habitat was dairy pasture with ryegrass/white clover/chicory/plantain rotations. This second collection was part of a project to estimate species richness of New Zealand pastures (M. McNeil pers. comm.).

The collection from Ballantrae Hill Country Research Station Southern Hawke's Bay, New Zealand (40°81′S, 175°85′E) was made in 1994 by extracting soil and leaf litter samples from pasture in a Tullgren funnel under heat and light.

Results

Altogether, from all four collections, 24 collembolan taxa have been recorded, of which 17 can be named to species or species group, the other seven only to genus (Table 1). Nine of the named species have already been recorded from New Zealand (Greenslade 2011) but the remaining eight species are new records for New Zealand. The eight new records are all named species, which are cosmopolitan or near-cosmopolitan in distribution and considered to be introduced species from Europe. (For definitions of exotic, introduced, native and endemic see Greenslade & Convey (2012).) Notes on their taxonomy, ecology and distribution are given below. They are only, or largely, found on land modified by human activities, as is also the case in Australia for these same species (Greenslade & Ireson 1986).

Only four of the named species, Protaphorura fimata (Gisin, 1952), Sminthurus viridis (L 1758), and Bourletiella viridescens Stach, 1920 and Bourletiella hortensis (Fitch, 1863) are considered to be pests as adults, and probably as juveniles, because they feed on clovers, pasture grasses, garden vegetable or gnaw roots. Sminthurus viridis is found throughout New Zealand where it has been present since at least 1929 (Dumbleton 1938). It is a sporadic pasture pest in New Zealand whereas in Australia it is an important pest of clover and lucerne (Scott 1984). The distributions of the other six named species already known from New Zealand (B. viridescens and P. fimata are new records) are not well known but all are introduced probably from Europe. Entomobrya multifasciata (Tullberg, 1871), which may be a complex of cryptic species, like S. viridis, almost certainly originated from Europe. Both species are found in southern Australia and Tasmania in exotic grasses (Greenslade & Ireson 1986). The eight named species not previously recorded in New Zealand are listed in the following, with taxonomic notes on one of the already recorded species, Hypogastrura vernalis (Carl, 1901). Some notes on their distribution and ecology, where known are also given.

Hypogastruridae

Hypogastrura vernalis (Carl, 1901) Hypogastrura rossi Salmon, 1941 syn. nov.

At the time of sampling, this species was not abundant. Although it has been recorded from New Zealand before (Davidson et al. 1997), the synonymy of Hypogastrura rossi Salmon with H. vernalis has not been documented before. Hypogastrura rossi has never been collected outside New Zealand and Salmon recorded it from only two localities—one was from a lawn in Kelburn, Wellington, and the other from newly dug soil at Karori (Salmon 1941, 1943), both human-modified environments. The species occurred around and under concrete paths where it was reproducing. It was controlled by the application of nicotine sulphate. The type of damage was not mentioned but it is unlikely that any ‘damage’ noted was caused by this species as Hypogastrura species feed on microorganisms on dead plant and animal material. Specimens in the type series of H. rossi in the Te Papa Museum were remounted recently, the synonymy confirmed and recorded here.

Hypogastrura vernalis is nearly worldwide in distribution and present in Europe and Australia. It is common in improved pastures in Australia and also on arable land when conditions are moist and cool. The habitats where Salmon records H. rossi in New Zealand are typical for H. vernalis in Australia and Europe. Newman (1970) recorded that H. rossi was most abundant in spring in pasture in New Zealand and that it had a preference for cool, moist conditions.

Tullbergiidae

Mesaphorura macrochaeta Rusek, 1976

The morphology of specimens agrees with the most recent descriptions of this species (Fjellberg 1998; Dunger & Schlitt 2011). The species is common in agricultural soils in Australia and is widespread in temperate climatic zones, reaching high latitudes of the Southern Hemisphere and Macquarie Island in the subantarctic (Greenslade et al. 2012). It is an easily dispersed, invasive species. As a minute, exclusively soil-inhabiting species that feeds on a variety of microorganisms, Mesaphorura macrochaeta was probably originally introduced to Southern Hemisphere and northern sites by human intervention in importations of soil and moss peat (Greenslade 2006). As a soil species, it is not collected by suction sampling but instead by Tullgren funnel extraction of soil, but it is certainly widespread in soils of modified environments in New Zealand. Adams (1971) and McMillan (1969) may have recorded this species as Mesaphorura krausbaueri Börner, 1901, which probably does not occur in New Zealand.

Brachystomellidae

Brachystomella platensis Najt & Massoud, 1974

This species was abundant in some of the samples. Although it has not been recorded from New Zealand before, B. parvula (Schäffer, 1896), with which it has been confused, was identified by Womersley (1937) from Davies' Bush, Brookby, Manurewa, Auckland in 1934 (EDP coll.) and Adams (1971) from pasture 80 km north of Wellington. It is close to B. platensis in some morphological features. However, the latter differs in the male having a secondary sexual character of six plumose spines ventrally on abdomen III, as noted in the original description of specimens from a grass lawn at La Plata, Argentina. Also, the figure of B. platensis in the original description and current specimens from Australia and Zealand all lack seta p3 dorsally on all abdominal segments, which is present in B. parvula. The mucro also is larger and broader in relation to the dens than in B. parvula, according to the figures and description of the latter species by Fjellberg (1998). These differences were not noted in the original description of B. platensis (Najt & Massoud 1974). Brachystomella platensis is common in Australia in improved pastures and also occurs on grasses and on some sites with native vegetation.

Onychiuridae

Protaphorura cf. fimata (Gisin, 1952)

This is another soil-living species that is common in moist, organic-rich horticultural situations around the world. It has been recorded damaging roots of pasture plants and legume crops and, if in high densities, can cause complete failure of seedling emergence. In Tasmania, under some conditions, it is a serious pest of poppies. Again Adams (1971) and McMillan (1969) may have recorded this species as Protaphorura armata (Tullberg, 1869).

Isotomidae

Folsomides parvulus Stach, 1922

This species is, like M. macrochaeta, a small, white species, that is common in agricultural soils in Australia and here shown also to occur in New Zealand but, unlike M. macrochaeta, is more restricted in distribution. It shows a preference for warmer, moist soils so is rare in southern climates such as experienced in Tasmania and has a predominately a pan-tropical distribution. It could be classified as a native rather than introduced species. There is some doubt as to whether one or several cryptic species are included under the name; this is an issue that DNA sequence analysis may be able to resolve.

Isotomurus maculatus (Schäffer, 1876)

Again, this is a common species in Europe in pastures and other modified environments and also occurs in Australia. Although there have been some suggestions that there are several cryptic species represented under the name, its specific identity has been confirmed using allozymes and mitochondrial DNA analysis by Carapelli et al. (1995), although these authors did not include Southern Hemisphere specimens in their work.

Entomobryidae: Orchesellinae

Heteromurus major (Moniez, 1889)

This species was common in some samples. The main body is not pigmented except for the eye spots, which are black. Although there are eight ocelli, two are reduced. The body is hook-shaped in that the head is at an angle of about 40° to the body. The latter is covered in scales, as are the antennal segments I and III, leg segments and furca. Antennal segment I is subdivided and V is annulated. The mucro is two-toothed and has a spine. The empodial appendage is lanceolate and the claw has three teeth. The macrochaetal distribution on all segments is identical to that described by Mari Mutt (1980) for this species except for two extra lateral ones on abdominal segment II and one on abdominal segment III, which seem not to have been figured by this author. This macrochaetal pattern is the same as for the Australian specimens.

Heteromurus major is native to the Mediterranean region of Europe but has also been recorded from Chile, Mexico and Guinea. In Australia, it has been found in Ballarat (Victoria) and south of Canberra (New South Wales), although neither location is in the Mediterranean biome of that continent. Exotic species often have the ability to tolerate climates that are not experienced in their native region. However, this may be because different biotypes or lineages are present as cryptic species. In fact, this may be the case for H. major; Porco et al. (2012), using CO1 analysis, detected seven lineages within the species each from different localities in France, Belgium and Spain.

The species has not been recorded from New Zealand before, although specimens of another near-cosmopolitan species, Heteromurus nitidus (Templeton, 1835), from New Zealand are in Te Papa Museum, Wellington, New Zealand. They were described by Salmon (1942) as a new species and new genus, Propemesira duo-oculata (Salmon 1942) but Salmon synonymised Propemesira (Salmon 1942) with Ptenura (Templeton, 1844) and the species was synonymised with H. nitidus by Mari Mutt (1980). Three of these specimens have been examined by Greenslade and it is confirmed that they belong to H. nitidus as they have a reduced ocellus number (two) on each side, unlike H. major, which has six to eight ocelli on each side. They were collected from a house in Wellington. Therefore, two widespread species of the genus Heteromurus occur in New Zealand—one in the North Island and one in the South Island. The alimentary canals of H. major specimens contained mainly fungal hyphae and spores, but pollen was also present.

Entomobryidae: Entomobryini

Entomobrya spp

Individuals belonging to this genus are abundant in exotic pastures in both Australia and New Zealand. They have been identified as Entomobrya multifasciata, E. lanuginosa or E. nicoleti previously. Although they vary in colour from almost completely white, to white with pair of dark posterior lateral spots to strongly banded, recent chaetotaxic evidence indicates they may all belong to a single species which varies in colour and is not present in the Palearctic (Greenslade, Jordana & Bacquero in preparation).

Bourletiellidae

Bourletiella viridescens Stach, 1920

This is the second Bourletiella species known from New Zealand pastures. It has been recorded as from Europe and North America where it is common in horticultural situations and gardens. It is also known from Australia, where it has been recorded feeding on live plants, such as cucurbits, albeit at low levels, but showing a high consumption rate on decaying plants. Although there is a photograph labelled B. viridescens from New Zealand (see Bellinger et al. 2012), the locality could actually be Tasmania and the identification is invalid as it was made only from a photograph.

Discussion

The most recent checklist of New Zealand Collembola comprised 380 species and subspecies belonging to 103 genera (Greenslade 2011). By far the greatest majority of these species were collected and described by Salmon between the years of 1940 and 1972. However, Salmon confined his collecting to native environments and carried out no systematic field work in environments modified by human activities. Few new records or descriptions of New Zealand Collembola have been published since Salmon's work apart from those by Adams (1971), McMillan (1969) and Davidson et al. (1997). The older records cannot be verified because taxonomic conceptions of several species have changed over the last 40 years. It is therefore not surprising that so many species common in these habitats have not been documented before. In total, the current authors recorded 22 species in New Zealand pastures, which is close to the year-long study carried out near Wellington by Adams (1968) who recorded 25 species. McMillan (1969) recorded 26 species in his year-long sampling of two pastures near Lower Hutt, South Island. Although half of McMillan's species were native, they were only in low numbers. In the studies by both Adams (1968) and McMillan (1969), the numerically dominant species were the same (Isotomina (now Hemisotoma) thermophila (Axelson, 1900), Hypogastrura sp., B. parvula).

The longer-term research project of which this paper is a part has recorded soil-surface Collembola densities of up to ca. 5000/m² and Adams (1971) recorded a mean density of Collembola as 5000 in September and 67,000/m² in June in pasture soil. Densities as high as or even higher than those found here are frequent, especially in countries to which Collembola species have been introduced. For example, Salmon (1943) recorded H. rossi (now H. vernalis) that ‘appeared in such enormous numbers that it could be swept up by the bucketful …’. It is clear, given these high densities, that Collembola are likely to make a significant contribution to soil ecosystem services (Lavelle et al. 2006) but their relative economic importance has not been properly quantified as is the case for many soil invertebrate taxa. This is a particular concern in New Zealand because the fauna of agricultural lands is so poorly known, as shown by the new records documented here.

Soil is a primary resource on which all biodiversity depends for nutrition. The soil fauna, especially detritivores, play an essential, often catalytic, role in returning nutrients to the soil and thereby facilitate uptake of these nutrients by plants for vigorous growth. A diverse range of detritivores and predators together with the microorganisms that are mainly the primary decomposers are essential to maintain ‘healthy’, that is highly functional, soils. Lack of knowledge of the composition of the soil fauna means that soils can decline in function without being detected. A decline in global taxonomic skills means that, although ecosystem services quantification techniques are increasingly well developed (Sandhu et al. 2012), species may suffer serious population declines or even extinction without their economic value to mankind being fully recognised. Together with the increasing intensification of agriculture worldwide and with associated rapid rates of biodiversity loss (Wratten et al. in press), lack of knowledge of the soil fauna, in particular quantitative data, is a serious concern. The New Zealand studies point clearly to a significant number of abundant Collembola species new to the country being identified for the first time but only as part of a preliminary sampling effort.

Acknowledgements

Thanks are due to Josephine Springett, Mark McNeill and Michael Cripps for specimens and to Melanie Davison for technical assistance.