Biodiversity and Conservation 3, 45-56 (1994)

The soil fauna: the other last biotic frontier HENRI M. ANDRt~ .1'2, M.-I. NOTI 2'3 and PHILIPPE LEBRUN 2 1Section of Entomology, Musde royal de l'Afrique centrale, B-3080 Tervuren, Belgium. eunit~ d'Ecologie et de BiogOographie, Universit~ Catholique de Louvain, B-1348 Louvain-la-Neuve, Belgium. 3Universit~ de Lubumbashi, Zaire.

Received 27 April 1993; revised and accepted 19 July 1993

Different approaches to biodiversity yield global totals as small as 3 million or as large as 80 million species. Erwin's calculation and estimation leads to an estimate of ca 30 million species and relies on four assumptions of which one concerns the ratio between the number of canopy insects and those found elsewhere, especially in the soil. A short survey of the microarthropods living in coastal sand dunes and collected with a new flotation method yielded amazing results. In spite of the severity of the habitat (low organic matter content and extreme dryness), the density of microarthropods varied between 175 000 and 1 400 000 individuals per square metre, i.e., densities 3 to 10 times higher than densities usually observed in any other type of soil. A total of 31 species was recorded, most undescribed and smaller than 200/zm. The consequences of these findings on the estimation of the number of species are discussed. It is suggested that the soil, including the deepest horizons and the rhizosphere, might constitute a huge reservoir for biodiversity.

Keywords: microarthropods; mites; collembolans; biodiversity; species richness; density; soil; sand; dune

Introduction

Erwin, 10 years ago, suggested that there are about 30 million insect species. Using an insecticidal fog to 'knock down' the canopy insects, Erwin and Scott (1980) found more than 1100 species of canopy-dwelling beetles from Luehea seemanni in Panama. From these data, Erwin (1982, 1983) concluded that most tropical arthropod species live in the canopy and extrapolated that there would be perhaps as many as 30 million tropical arthropod species. On the basis of the proposition that the tropical arboreal ecosystem was the last frontier in general knowledge of Coleoptera (Erwin and Scott, 1980), Erwin (1983) titled his paper 'Tropical forest canopies: the last biotic frontier'.

Erwin's calculation and estimation were discussed and analysed in detail by sub- sequent authors (Stock, 1988; Stork and Gaston, 1990; May, 1988, 1990). The chain of arguments used by Erwin relies on at least four areas of uncertainty (May, 1990):

(i) what fraction of the beetle (or other) fauna on a given tree species is effectively specialized to it?

(ii) do beetle species constitute the same fraction of insect faunas in the tropics as they do in better-studied temperate regions?

(iii) for each insect species in the canopy, how many other species are found elsewhere in or around a tree?

*To whom correspondence should be addressed.

0960-3115 © 1994 Chapman & Hall

46 AndrO et al.

(iv) how do we scale up from the number of insect species associated with a given tree in a given place to a global total?

We would like to address the third point. Erwin (1982) was laconic on that point and just wrote: 'Based on my own observation, I believe the canopy fauna to be at least twice as rich as the forest floor'. The statement is repeated by Erwin (1983). The ratio between the number of species found in the canopy and elsewhere was first questioned by Stork (1988) who suggested that there might be even more species in the ground fauna than in that of the canopy. May (1990) went further: he observed that the number of individual mites in the soil and leaf litter is typically an order-of-magnitude larger than the number of beetle individuals in the canopy. Thus he concluded that if the number of species bore a direct relation to number of individuals, then Erwin's estimate of one insect species elsewhere on the tree for every two species in the canopy would be out by almost a factor 10. Unfortunately, two factors make it difficult to determine the value of the ratio:

(i) most studies on tropical soils refer to the numbers of individuals, not to the number of arthropod species (e.g. Andr6 et al., 1992). As acknowledged by Usher (1988), soil biologists have been less inclined to recognize species, and frequently have not been concerned with the taxonomic basis of their science and it has become fashionable to regard the diversity of soil communities as so great that it would be impossible to identify all of the species that exist in them.

(ii) the few comparative studies between canopy and soil faunas in tropical areas mention surprisingly low densities in the soil. This may be explained in several ways: (a) many authors choose to consider only macroarthropods and ignore microarthro- pods (Stork and Brendell, 1992); (b) many authors ignore those arthropods in the soil below the depth sampled by their soil corer; (c) no 'perfect' extraction method likely to extract the arthropods as a whole is known.

To explore the richness of the soil fauna, we carried out a short sampling campaign in coastal 'fore dunes' near Montpellier, southern France. The sand dune fauna was selected for three reasons: (i) the extraction method efficiency approached 100% with sand samples tested in the laboratory (Andr6 and Noti, 1993), (ii) Collembola and mites were expected to be poorly represented due to the low organic content of the sandy soil, together with its unstable character (Wallwork, 1976), and (iii) the fauna was supposed to be simple enough to allow specific identification of all arthropod specimens collected.

Materials and methods

Sampling was carried out on 11 December 1991 at Carnon, near the city border with La Grande Motte. Sand samples were taken using a core device of 35 mm diameter which could be longitudinally opened and whose interior was wider than the cutting edge to relieve compression of soil. After digging three trenches in the sand, eleven 48 cm 3 samples were collected horizontally at different depths (from -10 to - 7 0 c m ) as indicated in Fig. 1. Two series of four samples were collected under marram grass and a third series of three under sand with no vegetation. Some soil properties for the three profiles are summarized in Table 1.

The extraction method is new and derived from a CC14 flotation method used in

Soil fauna: the other last biotic frontier

,rO, a a Foreshore >

47

..,q

B

Depth [ 20 cm

~ . ' v - '

C

" " l " , . " •

Figure 1. Diagrammatic cross-section through the dune with positions of the eleven samples along the three sampling profiles A, B and C. For each sample (48 cm 3) are given the number of individuals (n) and the number of species (s) recorded. Due to an accident during the mounting process, the number of species recorded in the sample marked (*) is seriously underestimated.

medical acarology (see details in Andr6 and Noti, 1993). All arthropods were mounted in concavity slides for identification under the microscope.

Results

Species richness

A total of 31 arthropod species was found. The species richness for each major group is given in Fig. 2A. Actinedid mites form the richest group with 11 species, among which

48

Table 1. Some soil properties and the arthropod density and richness observed in the three soil profiles illustrated in Fig. 1. Profiles A and B are under marram grass

Profile A Profile B Profile C

Water (%) 2.87 + 0.56 3.07 + 0.80 3.78 + 0.42 pH 8.44 + 0.13 8.57 -+ 0.06 8.55 _+ 0.04 Granulometry a 90.41 + 2.20 90.17 +_ 1.99 88.21 -+ 1.84 N (%) 0.02 + 0.01 0.04 _+ 0.02 0.03 +_ 0.01 C/N 3.00 _+ 1.83 2.00 + 0.82 1.67 + 0.58 Organic C (%) 0.14 +_ 0.07 0.11 + 0.00 0.09 + 0.03 Na + (mg 100 g - l ) 11.59 + 3.74 17.33 + 1.73 10.57 + 0.74 CO3 = (%) 28.43 + 4.67 24.78 + 3.74 26.70 + 2.96

Arthropod density b 1 378 552 175 Species richness 22 17 3

a% of particles within the class 100-250/~m. b thousands of individuals per square metre.

Andr~ et al.

A 2 1 1

[ ] Pauropoda [ ] Endeostigmata

[ ] Symphyla [ ] Other Actinedida

[ ] Gamasida [ ] Protura

[ ] Oribatida • Collembola

• Acaridida [ ] Insecta

Figure 2. Species composition of the sand fauna. (A) Number of species observed for each major group of arthropods. (B, C. D) pie-charts for the three profiles (A to C in Fig. 1) showing the relative abundance of the major arthropod groups.

Soil fauna: the other last biotic frontier 49

are six Endeostigmata. The second richest group is Collembola, also with six species. Figure 1 indicates the number of individuals as well as the number of species for each sample. The local richness under the marram grass is surprisingly high: as many as 20 species may coexist in a single sample of 48 cm 3 (i.e. 3.6 × 3.6 × 3.6 cm). In contrast, the arthropod community living in the sand with no vegetation is virtually monospecific (a nanorchestid mite). Figure 2B-D gives the composition by major groups for each series of samples. As the soil properties are similar in all three profiles, the differences between their species composition are probably due to the rhizosphere of the marram grass and the special interactions at root/soil interfaces (Coleman et al., 1988).

Density

From these data, it was possible to estimate the density, i.e., the number of individuals per square metre of dune (Table 1). In the sand with no vegetation, the density was the lowest with 175 000 individuals m -2. Under marram grass, the density reached 1 378 161 individuals m -2. Such high densities have never been observed previously in any type of soil. For comparison, recent data from the literature are given in Table 2. It must be stressed that even the density of the monospecific microcommunity found under bare sand is particularly high: the highest density of actinedid mites ever recorded is 117 340 individuals m -2 (see Table 1 in Luxton, 1981 and Table 21.2 in Kethley, 1990). The high densities observed under marram grass compared with those observed under bare sand indicate again the influence of the rhizosphere on the edaphic fauna.

Comparison of the densities observed in Montpellier with those in Table 2 is, however, uncertain since the sampling depth varies between authors. As we did not sample the upper 10cm of the sand, i.e., the most populated layer, it is probable that our microarthropods densities are still underestimated.

The vertical distribution under marram grass of major arthropod groups is illustrated in Fig. 3. The vertical distribution of collembolans and mites is roughly similar, in both groups, the density per dm 3 (or per litre) of sand tends to decrease progressively with depth. The density of collembolans varies from 1127 individuals dm -3 at -10 cm to 239 individuals dm -3 at -70 cm. These figures do not agree with previous observations. According to Poinsot (1966), collembolans were restricted to the upper 2 cm, at most the upper 10 cm. These figures also exceed all previous observations made in sand: densities published earlier varied from 0.5 to 18 individuals dm -3 (Thibaud and Christ- ian, 1989) and from 6 to 144 individuals dm -3 (Christian and Thibaud, 1988). The density of mites decreases more slowly with depth than that of collembolans: it varies, under marram grass, from 1123 individuals dm -3 at -10 cm to 468 individuals dm -3 at -70 cm. Under bare sand, the density of mites, which consist almost exclusively of Endeostigmata, varies between 457 individuals dm -3 at -35 cm and 104 individuals dm -3 at -60 cm.

Species size

Numbers of species are related to size classes (body length) in Fig. 4. The body length classes used follow Morse et al. (1988). The maximum number of species occurs in size class -10 (135-165/~m). By comparison, the smallest classes collected in studies using the same length distribution of arthropods are - 3 (Morse et al., 1988) and -1 (Basset and Kitching, 1991). There are few species in the larger size classes. A noteworthy exception is Gordialycus tuzetae Coineau, a spaghetti-like endeostigmatid mite which

Table 2. Density of microarthropods in some soils

Location Sampling depth (cm) Density and Biotope (number

m -2)

Reference

Rainforest, Seram, Indonesia

0-10 soil + leaf litter 3 000 Stork (1988)

Coastal marsh ? Western Korea soil 9 070 Yoshida et al. (1989)

Maize field, 0-5 Canada soil 15 900 Winter et al. (1990)

Desert, 0-10 Negev, Isra61 loes 26 500 Steinberger (1990)

Soybean field 0-2 Georgia, USA soil 30 000 Farrar and Crossley (1983)

Tropical Forest 0-10 Papua New Guinea leaf litter 40 000 Wauthy and Lebrun (unpub. data)

Secondary rain forest Rio Taruma, Brazil

0-7 yellow literite soil 70 000 Adis (1988)

River forest 0-2.5 Yangambi, Zaire soil 72 000 a Maldague (1961)

Rainforest 0-7 Luiswishi, Zaire leaf litter 110 000 Noti (unpub. data)

Cutaway peat 0-20 Clonsast, Ireland grass leys 147 721 Curry et al. (1989)

Grassland, 0-5 Ireland Soil + leaf litter 150 000 b Curry and Momen (1988)

Beach dune, 0-5 Georgia, USA soil 161 000 Mallow et al. (1984)

Beech forest, 0-15 Germany leaflitter 186 000 Schaeffer and Shauermann (1990)

Oakwood, 0-10 Meerdael, Belgium soil + leaf litter 195 000 Lebrun (1971)

Pine forest, 0-5 California, USA leaf litter, subsoil 220 739 Price (1973)

Alpine grassland, 0-15 Switzerland soil + leaf litter 386 000 Matthey et al. (1981)

aThis figure includes also annelids. bThis figure includes also macroarthropods.

Soil fauna: the other last biotic frontier 51

Figure 3. Vertical distribution of the major groups of arthropods in the sand dune under marram grass. The subgroups of mites are detailed in the foreground.

crawls into the sand and reaches a length of 2000 ym with a diameter of ca 50 #m. The two smallest species were a tarsonemid mite close to the genus Parapygmephorus (108/~m) and a nanorchestid mite (102/~m).

The data of Fig. 4 are skewed to the right for two reasons. First, it is based on dimensions of adults. Yet, most populations also included immatures. For comparison, a G. tuzetae adult is 2000/~m long (class +3) while its larva is only 845ktm (class -1). The most abundant acaridid mite measured 151ym (class -10) and 93 ~m (class -12), respectively at the adult and larval stase. The same ratio was found in a tydeid species (153 and 99#m respectively in the adult and the larva). Second, the probability of missing a small species is higher than that of missing a large species.

New species

From a systematic point of view, there is a clear cut difference between the micro- (less than 200/~m long animals) and the mesofauna (Fig. 4). Many of the species belonging to the mesofauna have been described and comprise psammophilous species such as the collembolans Doutnacia coineaui Massoud and Thibaud, Isotomina scappelifera Gisin, Isotomides productus (Axelson) or the endeostigmatid mites Gordialycus tuzetae Coineau, Nematalycus nematoides Strenzke, Micropsammus littoralis Coineau. In con- trast, not one species has been found to be described within the microfauna. This accords

52 A n d r ~ et al.

03 u.i 0 ILl O.. 03 IJ.. 0 n.. ILl rn

: : ) Z

-13 -12 -11 -10 -9 -8 -7 -6 -5 -4 -3 -2 -1 0 1 2 3 SIZE CLASSES

Figure 4. Distribution of the number of species per body length (adult dimensions). The body length classes used follow Morse et al. (1988). The two species for which only immatures were collected are not included. Double striped parts of the bars indicate the species that are described. The single striped part in class -10 refers to a species unknown at the time of the sampling but whose description was recently published (Fain et al., 1993).

with Gaston's (1991) conclusions that large species tend to be described earlier than small species and that taxa with large species are more completely described than those with small species.

Discussion and conclusions

Even if dune sandy soils are, in comparison with forest soils, much simpler in structure and much poorer in organic content, the sand dune fauna appears to be richer and denser than expected. Microarthropod densities are higher than those recorded in any other type of soil. The sand dune fauna colonizes the soil to a great depth (at least -70 cm); it is highly specialized (Coineau and Massoud, 1977; Coineau and Seely, 1983; Fain et al. , 1993) and composed of tiny species a large proportion of which are still undescribed. It is hard to believe that the endogenous fauna of highly organic soils would be less dense than that of sand dunes. On the contrary, we suggest that the forest soil fauna is much richer and denser than has been recorded so far but has been unnoticed for several reasons:

(i) Selective sampling. Most reports on the soil fauna do not include counts of microarthropods in the lower soil horizons (Seastedt, 1984). In other words, most published estimates refer only to the hemiedaphon, i.e., the part of the fauna that colonizes the surface organic layer, and neglect the euedaphon, i.e., the part that

Soil fauna: the other last biotic frontier 53

lives in the underlying mineral soil. Published densities typically range from 50 000 to 300 000 individuals m -2 (see Table 2) and represents hundreds of species in temperate forests. Furthermore, many reports on the soil fauna disregard also the epigeon (also called epiedaphic or epigeal fauna), i.e., the surface-dwelling arthro- pods usually collected with pitfall traps. Some thousands of arthropods may represent from 170 (Matthey et al., 1981) to 249 species (Schaeffer and Schauer- mann, 1990) compared with, respectively, 120 and 153 hemiedaphic species. A further example is taken from Villalobos and Lavelle (1990) who collected 7566 soil Coleoptera from a tropical grassland in Veracruz (Mexico) and identified 113 species for a mean density of 284 individuals dm -2.

(ii) Selective extraction method. Comprehensive accounts on extraction techniques have been published. The most popular method used for the study of the forest floor fauna is the Berlese-Tullgren funnel extraction. This technique is known to be inefficient for tiny mites such as Actinedida or other immature mites. Other techniques, such as hydrocarbon adhesion methods or flotation methods, are also used. Their real efficiency is generally unknown and may vary depending on the taxa collected and their size (see Andr6 and Noti, 1993).

(iii) Selective sorting and identification. Mites and collembolans usually account for 95% of the total microarthropods. Oribatid mites are the most often studied among Acari. However, smaller mites such as Actinedida are often neglected and rarely identified. Even in publications where they are considered, their real importance is probably underestimated since they live deep in the soil (and thus are not sampled) and are poorly responsive to funnel extraction. Yet, Actinedida may constitute by far the most abundant group as in the Negev desert (Steinberger, 1990). Price (1973) who studied the mineral subsoil in a Californian pine forest concluded that they were the most abundant and most diverse group. He found almost twice as many species of Actinedida as of Oribatida, a ratio similar to that we observed in sand dunes. Actinedida densities are also underestimated since they are tiny, delicate and colourless mites which are easily overlooked during the counting process.

If the forest soil fauna is at least as dense as that of the sand dunes, the number of individual microarthropods in the soil and leaf litter would not be an order-of-magnitude larger than the number of beetle individuals in the canopy as suggested by May (1990) but probably two orders-of-magnitude. If we accept a direct relation between the number of species and the number of individuals, this implies that Erwin's estimate of one insect species elsewhere in the tree for every two species in the canopy would be out by almost a factor of 100 times. This extrapolation is highly speculative and might be revised down if we consider that microarthropod densities in tropical forest are generally lower than those recorded for temperate forest soils (from 40 000 to 110 000 vs ca200000 individuals dm -2, see Table 2). The comparison between densities observed in Papua New Guinea (40 000 individuals m -z) and in Belgium (195 000 individuals m -z) is particularly illustrative as the same sampling and extraction methods were applied. However, species diversity in tropical soils is probably higher than in temperate forests (Wallwork, 1976). If we accept that Erwin's ratio is out by a factor 10, Table 7 of Stork (1988) should be corrected accordingly and the estimates of arthropod species in tropical rain forest should vary between 29 and 366 million species, a range so large that it becomes unrealistic.

54 AndrO et al.

The size of animals is also of importance in the debate on biodiversity since there is an empirical rule relating organism size to their species richness: for each tenfold reduction in length, there would be 100 times the number of species. However, this empirical relation begins to break down at body sizes below 1 cm in length. This break- down might be attributed to our lack of knowledge of small arthropods, most of which are undescribed. This hypothesis holds especially if we consider that the euedaphic fauna is virtually unknown (Lebrun and Wauthy, 1981). May (1988, 1990, 1992) extrapolated this rule down to animals of characteristic length of 200 Arm and arrived at an estimated total of around 10 million species of terrestrial animals. If we consider the euedaphic fauna, we are led to consider animals of characteristic length of 135-165/zm (size class -10) and to add another 10 million species to the total estimated by May, i.e., a total of 20 million species of terrestrial animals.

Based on these findings, many extrapolations and speculations may be made in order to estimate the total number of species found on Earth. The most important conclusion reached by this study is the importance of the edaphic fauna whose abundance exceeds all previous expectations. The importance of the edaphic fauna is again strengthened if we consider the whole soil microfauna (Protozoa, Nematoda, Enchytraeidae, Tardig- rada, etc.), the density of which is expressed in millions of individuals m -2. If the biosphere is viewed as a thin layer covering the earth, the canopy may be viewed as the upper biotic frontier of the terrestrial biota while the soil, especially the deepest horizons and the rhizosphere, forms the lower frontier. In the light of our results, it seems that the latter constitutes a huge reservoir for biodiversity, probably much more important than the former.

Acknowledgements

The senior author thanks S. Kreiter and G. Fauvel who provided him with laboratory facilities in Montpellier as well as D. Cotton, Adjoint-au-Maire of the city of Mauguio- Carnon for permission to work in protected areas. The authors also thank A. Fain, G. Wauthy, W. Karg for identification of special groups and J. Adis, D.A. Crossley, Jr and N.E. Stork for reading and commenting upon a first draft of this manuscript.

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