Annals of Arid Zone 45(3&4): 1-22, 2006 Australian Earthworms as a Natural Agroecological Resource 1 2 R.J. Blakemore and M. Paoletti 1 YNU, Tokiwadai Campus,Yokohama, Japan. 2 Department of Biology, University of Padova, Via. U. Bassi, 58/b, Padova 35121, Italy Abstract: Australia has an unrealized natural resource in its unprecedented diversity of earthworms. Surveys on the ground and of the literature give a total for Australia (and Tasmania) of 715 species and sub-species in 73 genera and ten families, comprising 650 endemic natives, wholly adapted to Australian climates and soils, and 65 (ca. 9%) exotic interlopers that tend to be less specialized, but more widespread. Of the exotics, just one-third, about 3% of the total species, are lumbricids of the holarctic family Lumbricidae. If neo-endemics and translocated natives are included as non-natives, it raises their numbers above 80 species – higher than a previous “National Survey” estimate of just 27 species. Compared to any other region, the earthworm fauna of Australia is particularly diverse (e.g. India – 350 spp., New Zealand – 200 spp.; USA/Canada – 180 spp.; USSR – 113 spp.; Amazonia – >120 spp; British Isles ca. 69 spp.) and, as much of the continent has yet to be systematically surveyed, it is anticipated that the tally of both natives and exotics will continue to grow many-fold. Earthworms are vital for sustainable primary production and waste management, yet only slowly do we gain an ecological appreciation of their potential to benefit Australia’s natural environment. Experiments and field trials in Australia have tended to mimic those conducted overseas, especially in Europe, using a limited range of exotic species, with similarly variable results and have largely overlooked native species. A long-term project to import the exotic Aporrectodea longa from Tasmania to the mainland was somewhat compromised from the outset by the well-documented prior occurrence, not only of this species, but also of many other ‘deep-burrowing’ species, on the mainland. However, it now seems that modifying soil to maintain or enhance conditions favorable for resident populations to recolonize and expand may prove the most beneficial option for both worm and farmer. Appropriate management strategies are briefly presented. Key words: Australian earthworm biodiversity, natives, exotics, soil management. Soil is not, then, something that is dead. are ubiquitous and amongst the most ancient It is teeming with a great variety of life of terrestrial animal groups. They play a forms ranging in size from the vital role in the formation and maintenance submicroscopic viruses, through bacteria, of fertile soils and are thus paramount for microbes, fungi, to the colossus of the various primary production (Fig. 1). Charles Darwin species of earthworms. A mere handful of (1837; 1881) was one of the first scientists warm, moist, fertile soil contains a life to give credence to the conventional wisdom population that is astronomical P.A. Yeomans from earlier civilizations about the (1958): Keyline Plan. importance of earthworms to soil fertility, and thus human survival. A resurgence in Earthworms, or the often larger interest in earthworms is driven by megadrile annelids of the class Oligochaeta, 2 BLAKEMORE & PAOLETTI Fig. 1. Effects on plants (Sorghum bicolor) and soil two weeks after five earthworms (Pontoscolex coethrurus) added to core on right-hand-side compared to control. [Photo Courtesty of Dr. Les Robertson, BSES, Tully]. environmental and economic concerns, Earthworms are a major component of particularly the need to understand and the soil macrofauna and as potential utilize their function in sustainable restorative agents or ecosystem engineers, agriculture, to exploit their potential for have significance in all these processes and recycling organic matter and as indicator roles, either directly (e.g. by working the species for environmental health (Lee, 1985; soil) or indirectly (e.g. by influencing Sims and Gerard, 1985, 1999; Buckerfield macro-, meso-, and micro- organisms). The et al., 1997; Paoletti, 1999; Blakemore, issues of soil physical properties, chemical 2002). fluxes, soil formation, plant production and Perhaps the most important functions decomposition, and soil biotic processes attributed to soil biota are: are all interrelated. The mechanisms and magnitudes of the contribution of • maintenance of soil structure, earthworms are reviewed elsewhere, e.g. • regulation of nutrient cycling processes, in Lee (1985), Blakemore and Temple- Smith (1996), and Edwards and Bohlen • direct interacting with plants and (1996). indirectly via microbial stimulation, • as indicator species of the state of health Earthworm communities comprise four of the soil ecosystem, and components (Blakemore, 1999; 2002): resident natives that are often highly • as alternative food source for insect endemic, translocated natives (i.e., endemics biocontrol predators. relocated within a bioregion), neoendemics • as bioprospecting resources for new (i.e., speciation in a new region after molecular or pharmaceutical products. introduction), and introduced exotics that EARTHWORMS AS A NATURAL AGROECOLOGICAL RESOURCE 3 tend to be less specialized and more taxonomic determination of collected widespread. Recent studies have revealed materials (to Family, Genus, Species, Sub- a previously unrealized Australian species levels) (Table 1). biodiversity of each of these groups while Compilation of Australian species also simplifying the taxonomic process, mapped by Abbott (1994) showed most without sacrificing phylogenetic relationships, in order to relieve field Table 1. Contingency table of sampling reliability taxonomists from the tedious requirements Case Sampling Taxonomy Results to obtain SEMs of modified setae (where 1 + + Representative data present), or a futile hunt for obscure (and 2 + – Unrepresentative data often absent) fine ultrastructural nephridial 3 – + Unrepresentative data minutiae. Much more reliance and 4 – – Unrepresentative data importance is placed on the condition of +, Good; -, Poor. the less environmentally adaptive reproductive organs, internal and external earthworms are reported from regions with structures define taxonomic groups and >400 mm annual rainfall, exceptions are allow resolution at all levels for the majority those from river basins such as the of species (Blakemore, 2005). Murray-Darling (see Blakemore, 2000b). But this may be a partial artifact of sampling The most important foundation of our effort, as arid regions tend to be understanding of species diversity comes under-represented in surveys due to logistic from field observation and taxonomic constraints and infrequent favorable periods. surveys, for earthworms, as with other Yet arid areas can support populations: groups, the outcomes are dependent of two sampling in temperatures >40°C, with soil factors: reliability of sampling methods and so dry and hard that a pneumatic drill competency of identification (Table 1). Too was required, Blakemore (1994; 1997a) often soil faunal surveys do not adequately discovered abundant natives, quiescent at sample e.g., using narrow diameter corers, depth under pasture in Queensland sub- or Tullgren funnels that miss larger tropics. specimens, yet report earthworms as Methods and Presentation “negligible” or “depauperate”; and smaller species may easily be misidentified or Data herein is compiled from field and classed as immature, whereas incomplete literature surveys extending over several identifiers, with only a few choices, force years and from reviews such as those just those choices. A solution is an “eco- presented by Lee (1985), Edwards and taxonomic” methodology aimed at Bohlen (1996) and citations in Blakemore (2005). The current paper will follow section overcoming both these deficiencies, as headings in a chapter of the recent update advocated and explained by Blakemore of “Earthworm Ecology” by Baker (2004) (1994; 2000; 2002), ISO 23611-1 (2006) titled “Managing Earthworms as a Resource and ICZN (1999). In brief, this involves in Australian Pastures” and offer responses adequate and representative ecological to some issues raised therein. sampling, combined with thorough 4 BLAKEMORE & PAOLETTI The Earthworm Fauna in Australia in 38 genera belonging to 4 families comprising: 202 natives (in 24 genera), Under this heading Baker (2004) states 1 new species (Blakemore unpublished) and “The earthworm fauna is dominated by exotic 1 neo-endemic (from Subantarctic species, most notably Lumbricidae…introduced accidentally from Macquarie Island), 3 translocated mainland species and 23 exotics that have several Europe” and “Thus, the most common cosmopolitans in common with the mainland earthworm species in disturbed land in (Blakemore, 2000a,b,c; 2004). Both exotics Australia are the peregrine lumbricid and natives, e.g. several Anisochaeta, species..” These statements are misleading Anisogaster and Megascolides spp., were as, from a total Australian fauna now known found on farms and under pasture. to comprise 715 species, only about 65(9%) are exotics and, of these, only a third (or Many more species await description, about 3% of the total) are from the holarctic e.g. Abbott’s (1985b) collection from the family Lumbricidae. Possible reasons why Jarrah forests of WA in the Museum of these exotics are claimed to be dominant Natural History, London, number more than is due to lack of adequate sampling and/or 60 morpho-species (pers. obs. RJB, 1996), identification skills as confirmed by and further field surveys and sifting through quantitative and qualitative sampling in the shelves of Museum collections will various regions of Australia, from sub- undoubtedly reveal many new, undescribed antarctic to sub-tropics, where lumbricids species that will, naturally, not be listed were found frequently, but as just a anywhere and for which specialist help is component, whether in managed or needed. Thus it can be anticipated a total unmanaged habitats. These results are fauna for Australia to increase many fold summarized in Blakemore (2005) where the to eventually number several thousand taxa. 715 taxa in 73 genera and 9-10 families represent the most complete and Australia thus has a much greater natural comprehensive checklist of Australian resource base of earthworm species than earthworms. About 650 are natives in 45 available in most other regions of the Globe, genera in just 3 or 4 families plus 10 or and it is perhaps less appropriate to emulate 12 possible neo-endemics, fully adapted to studies from North America (that has less Australian climates and soil conditions, and than 200 earthworm species in total - another 64-65 species are cosmopolitan Blakemore, 2005) or Northern Europe e.g. exotics that often have broad tolerances and British Isles with just 69 recorded species worldwide distributions (Blakemore, 2002). (although ca. 20 of these were from Botanic Of these exotics about 20 are new national Gardens - see Blakemore, 2005), where or state records from the senior author’s climatic and edaphic conditions differ and studies including the first Australian report the faunas are more limited. What is needed of Lumbricus terrestris Linnaeus, 1758, but is an initiative to re-evaluate and to fully many of the new records are for smaller appreciate the unique conditions and species species. combinations available for original study These national figures naturally include in the context of Australian soils and the 230 native and exotic Tasmanian species conditions. EARTHWORMS AS A NATURAL AGROECOLOGICAL RESOURCE 5 Identification Guides to Australian are no unified keys or guides to Australian Earthworms earthworms, as there are for Australian microdriles (small, aquatic worms), i.e. For fieldworkers, the difficulties of Pinder and Brinkhurst (1994), or for New collecting and identifying specimens, due Zealand earthworms (Lee, 1959; to lack of adequate identification tools, are Blakemore, 2005). Figure 2 shows some compounded by the problems of family characteristics. Presently, several differentiating native from exotic species resources must be consulted to identify the and of knowing the full extent of those species. In summary: exotic species that are present. Identification of earthworms requires magnification, some Blakemore (1994), attempted a complete dissection at certain stages, and a reliable eco-taxonomic guide to Australian natives guide to the proven (and potential) species. and exotics that is still useful, but the Just giving a choice between half-a-dozen taxonomy now needs upgrading. species will force only those choices; while Blakemore (2000d) described 230 omitting potential species, such as regional natives and exotics from the island state cosmopolitans or those from adjacent lands, of Tasmania and keyed them with an help ensure their continued omission. For interactive (DELTA) computer guide. instance, an “Earthworm Identifier” by Jamieson (2000) covered 404 Australian Baker and Barret (1994/5) appears to be Megascolecinae, most in superceded based on a guide to the British fauna by combinations, yet omitted ca. 200 spp, Sims and Gerard (1985) and identified only despite a 2001 revision “Supplement”. a dozen (mainly lubricid) species, or less than 2% of currently known Australian Dyne and Jamieson (2004) reviewed species, but still managed several critical native (and inadvertently several exotic) errors while also giving the allusion Acanthodrilidae, Octochaetidae, and persisting from 19th Century literature that (doubtfully) Exxidae, erecting some names the main species were “the common with invalid designations that must be European earthworm”. Unfortunately, there ignored; incidentally; this publication makes Fig. 2. Major earthworm families: 1 Acanthodrilidae, 2 Megascolecidae, 3 Lumbricidae (from Lee et al., 2000 after Lee, 1959 Tuatara VIII(1): figs. 1-3). 6 BLAKEMORE & PAOLETTI no reference to “ecology” for any of these known fauna and, of the exotics known species. even then (e.g. Blakemore, 1996a or b, 1997a or b), these represented just about Blakemore (2002) presented a complete half (Baker et al., 1997). This data will guide to taxonomy, ecology and world also under-represent deep-burrowing distributions of about 120 most common species. exotics, including all those known from Australia, and an update volume is in Australia’s neo-endemics are found in preparation. these (families and) genera: Blakemore (2005) updated and corrected (Megascolecidae) Pontodrilus with a list (publicized via ABRS, 2004) – and uncertain origin, (Megascolecidae) this new species checklist is the most Begemius from New Guinea, complete and current tally of names. (Octochaetidae) Octochaetus from New Zealand, and (Acanthodrilidae) Rhododrilus Species Diversity and Biodiversity and Maoridrilus also from New Zealand, Results for Australia that, if counted as exotics, would raise the total of non-natives from Australian In more urbanized or disturbed states to about 80 species. environments a few species can be collected on topsoil just digging down 20 cm. Among Although patchily sampled, high the commonest species the ones in Plate diversity has been recorded from some 1. But if the cores are made in shelterbelts Australian sites – incomparable to habitats and hedgerows (such as in the area of elsewhere in the world. For example, from Gerangamete, Vic) some additional native a total of about 40 species identified during species can be added (Plate 1 a,b). three years’ observations around Brisbane A selection of Australian abundance and in Queensland, 24 species (16 exotics + diversity studies is presented in the table 8 natives) were located on and adjacent below (Table 2) which can be compared to a farm at Samford in south-east to results from other regions. Use of faunal Queensland (Blakemore 1994; 1997a); 24 guides and collection methods more suitable species (5 exotics and 16 natives plus 3 for Europe appears to have yielded limited microdriles) were collected one week on results in local surveys of parts of some the shores of Lake Pedder in the Tasmanian southeastern Australian states (Baker, Wilderness World Heritage Area 2004), whereas an ambitiously titled (Blakemore, 2000a); and sixteen species "National Survey of the Earthworm Fauna (10 exotics and 5 natives plus an of Urban and Agricultural Soils in Australia" enchytraeid) were found after a couple of based on superficial samples supplied by weekends’ surveys on a 45 ha property schoolchildren and a northern European in the Southern Highlands of NSW guidebook (viz. Sims and Gerard, 1985) (Blakemore, 2001c). While the average tried to identify specimens for which "no Australian backyard garden can support a dissections were attempted" and yielded varied community, often of about a dozen predictable results: just 27 mainly lumbricid species, both known and new (e.g. taxa, or just about 4% of the currently Blakemore, 1997a; 2000d). EARTHWORMS AS A NATURAL AGROECOLOGICAL RESOURCE 7 PLATE 1.Some easily found earthworms in Victoria: a,b - Native perichetine earthworm Anisochaeta macleayi (Fletcher, 1889) found in Gerangamete forest VIC. and nearby shelterbelts, c- Introduced very common species Lumbricus rubellus, d- Introduced species les common than the previous one has been found in one organic orchard in Melbourne, e- Introduced earthworm Octolasium cyaneum common in pastures, orchards with This diversity is mainly due to and have accompanied these crops via the persistence of natives, combined with spread of agriculture and world trade, contributions from the pool of exotics although transportation of earthworms to originating from various temperate and regions they are not native to, as with tropical regions of the world - where their the crops, is not necessarily direct. As origins often correspond to the eight evidence for this, the faunal lists for the independent centers of the world’s major Levant and Maghreb will have many names cultivated plants (Vavilov, 1951). These familiar to workers in other regions of the earthworms may well be attendant upon globe (see Pavlicek et al., 2003; Omodeo 8 BLAKEMORE & PAOLETTI Table 2. Summary reports of diversity and abundance in various Australian habitats (some are totals rather than mean values) – references in Blakemore (1994; 2002) State or Habitat TaxaA Total Nos. Biomass Reference Territory spp (m-2) (g m-2) SA wheat/fallow exotics 3 20-450 2-74 Barley (1959) SA Pasture exotics 3 260-640 51-152 Barley (1959) NSW alpine forest natives 10 7-135 1.2-81.8 Wood (1974) Vict. Woodland natives? N/A 25-195 N/A Ashton, 1975 Vict. Orchard sexotics and 5? 0-2,000 N/A Tisdall, 1978 natives Queesland Rainforest natives? N/A 140-150 N/A Plowman, 1979 WA Wheatbelt exotics 4 N/A N/A Abbott and Parker, 1980 Vict. Pasture lumbricid 5 15-21 N/A Tisdall, 1985 WA jarrrah forest natives 7 + 62 4-91 0.3-27.0 Abbott, 1985a; spp. 1985b WA Pasture exotics 5 19-157 8-61 Abbott, 1985a WA Pasture Native 1 N/A 30-96 Abbott et al., 1985 SA Wheat lumbricid 1 130-341 21-100 Rovira et al., 1987 Vict/NSW Pasture/crops exotics and 9 0-802 N/A Mele, 1991 natives Queesland Barley lumbricid 1 9-54 0.3-5.3 Thompson, 1992 WA Pasture exotics 2 58-170 20-90 McCredie et al., 1992 Quessland Pasture natives and 6 0-1,020 0-31.1 Blakemore, 1994 Narayan exotics Quessland Arable exotics and 24 0-263.8 0-68.1 Blakemore, 1994 Samford natives Macquarie Isl. Natural exotic and 3 NA NA Blakemore, 1997 neo-endemic Tas. L. Pedder Sclerophyll Natives, 24 NA NA Blakemore, 2000b wilderness exotics and translocated spp. NSW Pasture exotics and 16 NA NA Blakemore, 2001c natives Highest Totals – 24 2,000 152 – A exotic or introduced taxa are from various families; natives are mainly megascolecids, or in Queensland, megascolecids, octochaetids, and acanthodrilids. N/A - data not available. et al, 2003). However, it is important to Contrasting to these recent higher realize that native species are unique and Australian figures, Lee (1985) and Lavelle fully adapted to Australian habitats. and Spain (2001) say that earthworm EARTHWORMS AS A NATURAL AGROECOLOGICAL RESOURCE 9 communities from a wide variety of regions south (e.g. Blakemore, 1997a,b; 1999). and habitats rarely comprise more than 8-11 Overviews of sustainable productivity and species, most commonly just two to five, earthworm effects in drylands and tropics, which Baker (2004) paraphrases as: “more including in the Australian region, may commonly only two to three species are be found in Pearson et al. (1995) and Brown found”. et al. (1999). The highest abundance for Australian Programs to Redistribute pastures are equivalent to 6.4 million worms per ha and 1.52 t ha-1 (Barley, 1959) which Earthworms is a biomass value higher than the usual Earthworms occur naturally in all soils stocking rate of a pasture. In comparison, except where recent volcanism, glaciations, a 1,000-year-old permanent pastures in UK inundation or desertification precludes them. stabilized with a winter population of six Agricultural management practices that lumbricids at 4.6 million worms per ha remove native vegetation with cultivation and 1.53 t ha-1 (Blakemore, 1981; 1996; and the introduction of exotic crops or 2000c). pastures, or use of toxic biocides can also deplete indigenous faunas. Thus it is only Earthworms in Pastures in in virgin soils (e.g. post-glaciations), land Northern Australia reclaimed from oceans such as the Dutch Under this heading Baker (2004: 277) polders, recently cleared lands (e.g. states “Very little is known..” and as Brigalow in Quessland or pastures in New evidence cites Baker et al. (1997) Zealand), or those subjected to intensive documenting the exotic Pontoscolex agriculture that have impoverished corethrurus, although accepting that earthworm populations. There are many Blakemore (1997a or b) reported that the reports, from around the World, of introductions of exotic and native earthworm earthworm (re-)introductions into these species increased pasture production on kinds of soils to stimulate productivity or brigalow soils by 64% within a year in to rehabilitate degraded soils. Unlike trials southeastern Queensland”. The number of in other countries, introduction attempts in species tested in extensive ecological Australia have not generally been preceded experiments in the laboratory, glasshouse, with glasshouse trials (except those and two medium-scale field trials in pastures conducted by Blakemore, 1994), but just by Blakemore (1994; 1997a) were over like other countries, use of lumbricids has 30 that resulted in pasture increased of yielded variable results. Findings from such 26% and 64%. Intensive preliminary surveys trials are summarized in Tables 3 and revealed presence of greater than 75 species 4. from the southeast Queensland study area. Stockdill (1966; 1982) as reported by From the whole of the Northern Territory Lee (1995) documented pioneering work only about 20 species are currently known done in New Zealand on the effects of (listed by Blakemore, 2005), about the same introduced lumbricids on the productivity number as found in a single farm in the of pastures which lacked them whereby 10 BLAKEMORE & PAOLETTI Table 3. Summary of pot experiments of earthworm effects on plant yields (references in Blakemore, 1994) Workers Dates Country Spp. Plants Controls (%) Wollny 1890 Germany lumbricids crops useful effects Russel 1910 U.K. lumbricids ? 25% Hopp and Slater 1948 U.S.A. lumbricids hay/clover 48-95% Hopp and Slater 1949 U.S.A. A. caliginosa/ millet 11% NS Diplocardia sp. lima beans 8% NS soybean tops 248% wheat grains 20% Nielson 1951/3 N.Z. lumbricids turves and 31-110% grass Waters 1951 N.Z. A. caliginosa rye grass Ponomareva 1952 U.S.S.R. ? crops 400%? Zrazhevskii 1958 U.S.S.R. A. caliginosa tree saplings 26% and 37% Atlavinyte et al. 1968 U.S.S.R. lumbricids barley 92-201% VanRhee 1965 Holland A.. longa/ grass, wheat 287%, 111%, L terrestris clover 877% Marshall 1971 U.S.A.? A. caliginosa/ L.terrestris black spruce significant 1 yr. Atlavynte/Pocine 1973 U.S.S.R.? A. caliginosa oats 20-50% Aldag and Graff 1975 Germany? Eisenia fetida oat seedlings 8.7% (21% protein) Edwards and Lofty 1978/80 U.K. 4 lumbricids barley increases Graff/ Makeshin 1980 Germany lumbricids ryegrass 10% Abbott and Parker 1981 Australia A. trapezoids ryegrass -23% Atlav./Vanagas 1982 Lithuania A. caliginosa/ barley grain 4-220% L. terrestris Mackay et al. 1982 N.Z. A. caliginosa/ L. rubellus ryegrass 2-40% McColl et al. 1982 N.Z. A. caliginosa ryegrass 5-50% Atlavinyte and 1985 Lithuania A. caliginosa barley 56-96% Zimkuviene James and 1986 U.S.A. A.caliginosa/ bluestems -7-18% Seastedt Diplocardia sp. Kladivko et al. 1986 U.S.A. L. rubellus corn seedlings greater emergence Sharma and Madan 1988 India worms abd wheat/maize slight dung Haimi and Einbork 1992 Finland A. caliginosa birch 200% in 119 days Haimi et al. 1992 Finland L. rubellus birch 28.5% in 1 yr Spain et al. 1992 Africa 5 tropical spp maize -12%-154% 3 tropical spp panic grass -10%-214% Pashanasi et al. 1992 Peru P. corethrurus tree seedlings -80%-2,300%* Blakemore 1994/97 Australia 28 spp. various crops/ see reports grasses *Herbivory of control compromised results of Pashanasi et al. (1992).