Biodiversity of soil microarthropods: the filtering of species

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1 Biodiversity and Conservation 5, (1996) Biodiversity of soil microarthropods: the filtering of species HENK SIEPEL Institute for Forestry and Nature Research, P.O. Box 23, 6700 AA Wageningen, The Netherlands Received 10 October 1994; revised and accepted 27 January 1995 Decline of soil microarthropod biodiversity is described in the sequence: old forest stands, low-input grasslands, high-input grasslands (with and without the use of persistent pesticides). With this expected trend of declining biodiversity, the patterns of species losses are analysed with the use of classifications of life-history tactics, feeding guilds and tolerances to drought. Species intolerant to drought are absent in grasslands, but present in old forest stands. Also the fraction of thelytokously reproducing microarthropods is higher in old forest stands compared with low-input grasslands. The main difference between low-input and high-input grasslands is found in the feeding guild structure of the community. Low-input grasslands are dominated by (herbo-) fungivorous grazers, whereas high-input grasslands are dominated by fungivorous browsers. Application of DDT in high-input grasslands shows a high density of microarthropods with a high fraction of thelytokous reproduction, associated with a decrease in genetic variation in a thelytokously reproducing species. Patterns in species losses, the species filters, are explained and discussed. It is shown that the decline of biodiversity is not a random loss of species but follows an identifiable pattern. Keywords: mites; springtails; life-history tactics; feeding guilds; tolerance to drought Introduction Diversity of soil microarthropods has impressed many soil biologists and Anderson (1975) was among the first ones to formulate hypotheses to explain the enormous diversity. More recently Crossley et al. (1992) drew attention again to soil microarthropod diversity in relation to management practices and soil processes, Maybe in these two papers the keywords in biodiversity are formulated: explanation and management. In this paper I discuss both those keywords. I realize, however, that there is a long way to go before we understand soil animal biodiversity, let alone manage it, but let us begin. Soil microarthropods in Dutch soils usually comprise the mite orders Oribatida, Acaridida, Actinedida, Tarsonemida and Mesostigmata, with occasionally some Metastigmata. Also included are the insect order Collembola and a few species of Protura, Diplura and the myriapod order Symphyla. Other arthropod groups are either too rare or not taken into account, although many soil insect species fit in the size range of microarthropods. This precise definition of what is considered a soil microarthropod species is necessary in a paper dealing with biodiversity of such a group. Soil microarthropods are very numerous; species numbers up to 45 per 500 cm 2 have been found in Central-European forests (Moritz, 1965) and up to 26 per 5 cm 2 in Finnish forests (Karppinen, 1958) for oribatid units only. Total numbers of microarthropod species must Chapman & Hall

2 252 Siepel be even higher. Such a group must be ideal for studies in biodiversity, but only when the problem of identification can be overcome. Recently, Hengeveld (1994) presented a discussion paper on biodiversity in which he recognized several phases of degradation of biodiversity with increasing human influence in the environment. The first phase is the cutting of virgin forest for small scale agricultural practice. The land receives low inputs and yields low production of food. The second phase is the more intensive use of the land resulting in high inputs of fertilizers and frequent harvesting to obtain higher production of food or fodder on a regional scale. In the third phase, production is increased even more by the use of fast-growing races of plants and pesticides on almost a global scale. This process has been going on in Europe for more than 3000 years. Application of the newest technologies is now taken up in many parts of the world and at an increasing speed, It leads not only to a decrease in diversity of races for food or fodder, but also threatens diversity of other life forms. In the Netherlands it is no problem to find examples of high-input agricultural practice, including the use of pesticides. Low-input agriculture is not so easily found, while virgin forests are absent. The last virgin forest was cut in the 1980s. The next best are old forest stands (forested for at least 1100 years from historical sources: Ten Houte de Lange, 1977). These forests have been subject to restricted human influence, so they are not virgin, bu! are thought to have the least affected soil microarthropod community. The goal of this paper is not only to show that species diversity declines through the series: old forest stand, low-input grassland, high-input grassland (with and without pesticide use), but also to demonstrate that this decline is not random, that it follows a pattern. In every phase as described by Hengeveld (1994) a fraction of the total number of species will disappear because their life history tactic, feeding guild or range of tolerances becomes unfit for the new situation. The identification of these patterns, which I will call species filters, may give a better insight into the mechanism of declines of biodiversity and perhaps eventually into ways to prevent further declines. Materials and methods All sites investigated are situated on the Veluwe in the central part of the Netherlands and originally had about the same type of soil, a Haplohumod (Soil Survey Staff, 1975) developed in sandy material on a lateral moraine. Clay fraction is very low (<1%) and phko ranges from 4.0 to 5.0 in the unmanaged sites, but has become somewhat higher in the agricultural sites due to fertilization (Tischler, 1965). In this paper, data of former investigations on grassland microarthropods are re-used (Siepel and Van de Bund, 1988) and extended with new data from old forest stands. Because the forest sites could be sampled only in May, only May-samples from the older datasets have been used in these analyses. The Bovenbuurt grassland and Droevendaal grassland sites were sampled in May 1985 (Siepel and Van de Bund, 1988). The sites of the Plant Protection Service at Wageningen were sampled in May 1986 (van de Bund, unpublished data) and the old forest stands "Loenense bos', 'Ugchelense bos' and 'Hoenderloose bos' were sampled on 3 May At all locations four samples of 100 cm 3 (5 cm depth, O 5 cm) were taken and transferred directly to a Tullgren funnel, where soil microarthropod extraction from the samples took one week. Specimens were collected in 70% alcohol and transferred to lactic acid on microscope slides by hand. Specimens were identified to the species level although some

3 Biodiversity of soil microarthropods 253 rare actinedid species could not be given scientific names. The complete dataset thus consists of lists of identified species (with their numbers) of three old forest stands (Loenense, Ugchelense and Hoenderloose bos), three low-input grassland sites (50kgNha-ly -1 Bovenbuurt grasslands), and three high-input grassland sites (400 kg N ha -1 y-1 Droevendaal grasslands). The site of the Plant Protection Service at Wageningen had also received a yearly amount of DDT and, in 1986, 30% of the total amount (including derivates) ever applied was still present (Martijn et al., 1993). Data on genetic variation (as determined by esterase variation) of a dominant species in this site are used to demonstrate the decline in genetic variation within a species. Results Densities of individuals (expressed as numbers per m 2) and numbers of species are given in Table 1. Species numbers between forests and low-input grasslands, and the latter and high-input grasslands differ significantly (F-test: p < for both comparisons). So biodiversity is decreasing as expected in the sequence old forest stand, low-input grassland, high input grassland. The aim now is to identify the possible causes of decrease. Species and their numbers are grouped for each site according to their life-history tactics (Siepel, 1994, 1995), their feeding guilds (Siepel and de Ruiter-Dijkman, 1993; Siepel and Maaskamp, 1994), and their tolerance for drought (unpublished data). The characteristics for the identification of life-history tactics, feeding guild and drought tolerance are given for the abundant species at each site (a species is called abundant when its number exceeds 5% of the total number per site). References for the allocation to life-history tactics are given only for departures from the generally assumed pattern: sexual reproduction, no special traits for bridging unfavourable periods or distances (such as respectively diapause forms or dispersal abilities). Grouping in feeding guilds is based on Siepel and de Ruiter-Dijkman (1993) unless otherwise mentioned, and is restricted to data on mite~. Grouping in classes for drought tolerance is based on unpublished data and refersto oribatid mites only. Abundant species in at least one of the forest sites are: Brachychthonius berlesei (sexual reproduction, herbofungivorous grazer (unpublished data), avoiding drought), Platynothruspeltifer (a long living thelytokous species (Taberly, 1987), herbivorous grazer, tolerant to drought), Tectocepheus velatus (thelytokous (Grandjean, 1941), opportunistic herbofungivore, avoiding drought), Oppiella nova (thelytokous (Woodring and Cook, 1962), fungivorous grazer (unpublished data), avoiding drought), Microppia minutissima (thelytokous (Taberly, 1987), fungivorous grazer, avoiding drought), Nanorchestes arboriger (sexual reproduction, fungivorous grazer), Isotoma viridis (sexual reproduction), Isotomiella minor (thelytokous (Petersen, 1971)), and Folsomia quadrioculata (sexual reproduction). Abundant species in at least one of the low-input grassland sites are: Tectocepheus velatus (see above), Berniniella bicarinata (sexual reproduction, fungivorous grazer, avoiding drought), Ramusella clavipectinata (sexual reproduction, fungivorous grazer, avoiding drought), Liebstadia similis (sexual reproduction, herbofungivorous grazer, tolerant to drought), Scheloribates laevigatus (sexual reproduction, fungivorous grazer, tolerant to drought), Minunthozetes semirufus (sexual reproduction, herbofungivorous grazer, avoiding drought), Trichoribates trimaculatus (sexual reproduction, herbofungivorous grazer, tolerant to drought), Achipteria coleoptrata (sexual reproduction, herbivorous

4 254 Siepel grazer, mesotolerant to drought), Onychiurus bicampatus (sexual reproduction), lsotoma notabilis (see above), Isotoma viridis (see above), and Folsomia quadrioculata (see above). Abundant species in at least one of the high-input grasslands are: Dendrolaelaps strenzkei (facultative phoretic (Karg, 1971), general predator (Karg, 1971), Rhodacarellus silesiacus (sexual reproduction, general predator (Walter et al., 1988)), Pygrnephorus blumentritti (facultative phoretic (Lindquist, 1986), fungivorous browser (Krczal, 1959), Scutacurus quadrangularus (facultative phoretic (Lindquist, 1986), fungivorous browser), lsotoma viridis (see above), lsotomodes productus (sexual reproduction), lsotomurus palustris (sexual reproduction), and Proisotoma minuta (sexual reproduction). Abundant species in the high-input grassland with DDT application are: Oppietla nova (see above), Mesaphorura krausbaueri (thelytokous reproduction (Petersen, 1971), and Folsomia fimetaria (thelytokous reproduction). In Fig. 1 distributions of the microarthropods among life-history tactics are presented for the sites investigated. The life-history tactics are labelled by roman figures as in the original classification (Siepel, 1994) and are given a short, and hence incomplete, characterization in the legend. The main differences between the forest sites (Fig. 1, a-c) and the low-input grassland sites (Fig. 1, d-f) are the decreasing fraction of thelytokously reproducing animals (tactic X) and especially the long-lived ones among them (tactic IX). The relative increase in sexual reproducing individuals is indeed relative as we consider the decreasing total density of microarthropods (Table 1). The differences between the low-input and high-input grasslands (Fig. 1, g-i) are best characterized by the enormous increase in the fraction of phoretic species; either facultatively phoretic (tactic II), or obligately phoretic as adults (tactic IV). The effect of DDT-application on such a high-input site is shown in Fig. 1, j; a revival of the thelytokously reproducing individuals in high densities, but with a very restricted number of species (5 out of 23; Table 1). Also diversity within species is lower on this polluted site compared with reference sites. Only one clone of Oppiella nova could be identified on this site using electrophoresis of esterases, while clonal diversity on reference sites with even much lower densities was significantly higher (unpublished data). In Fig. 2 distributions of the mites among feeding guilds are presented for the sites investigated. Data allowing the distinction between fungivorous grazers and browsers are not yet available for Collembola. Differences between the forest sites (Fig. 2, a-c) and low-input grasslands (Fig. 2, d-f) are relatively small compared to the differences between low-input and high-input grasslands (Fig. 2, g-i). The main difference between forest sites Table 1. Average densities of microarthropods (in thousands m 2) and species (with SE) of the investigated forest sites, the low-input grassland sites, the high-input grassland sites, and the high-input site with DDT application Sites Density of Number of individuals species Forests _+ 5.3 Low-input grasslands _ _ 1.5 High-input grasslands 33.6 _ with DDT application

5 Biodiversity of soil microarthropods a v..ll III Iv tl u lu d. III g L I V Xl ~~IJ'~V Xl X'/I)'' h Xl X XvIV V J Xl II III IVy, X LEGEND XI XII I~1 X IX,, ~viv BRIEF LEGEND I II III IV V VI VII VIII IX X Xl Xll Parasites Facultative phoresy Obligate phoresy as juveniles Obligate phoresy as adults Obligate diapause Facultative diapause and semelparity Facultative diapause and anemochory Quiescence or facultative diapause Thelytoky and longevity Thelytoky Sexual reproduction Sexual reproduction and seasonal iteroparity VII VI Figure 1. Life-history tactics of microarthropods in old forest stands (a-c), low-input grasslands (d-f), high-input grasslands (g-i), and a high-input grassland with application of DDT (j). Tactics are described in detail by Siepel (1994), the legend gives a brief characterization.

6 256 Siepel a b C d ~ e z f g 11 h 11 i 11 LEGEND BRIEF LEGEND 1 fungivorous browser 2 fungivorous grazer 3 herbivorous browser 4 herbivorous grazer 5 herbo-fungivorous grazer 6 omnivore 7 opportunistic herbo-fungivore 8 arthropods predator 9 bacteriovore 1 0 ~ ~ 1 ~ 3 10 general predator 11 nematods predator 12 parasite Figure 2. Feeding guilds of mites in old forest stands (a-c), low-input grasslands (d-f), high-input grasslands (g-i), and a high-input grassland with application of DDT (j). Non-predatory guilds are defined by Siepel and de Ruiter-Dijkman (1993), predatory guilds are derived from Karg (1971).

7 Biodiversity of soil microarthropods 257 and low-input grasslands is the decrease of the fraction of fungivorous browsers (1) and the increase of that of general predators (10). The striking difference between low and highinput grasslands is the increase of the fraction of general predators (10) and fungivorous browsers (1) and the almost complete absence of fungivorous (2) and herbofungivorous grazers (5). Contrary to the otherwise comparable high-input grasslands, the DDT application site shows a very limited fraction of the several predator guilds (8, 10, 11) and a higher fraction of fungivorous grazers (2), but not of herbofungivorous grazers (5). In Fig. 3 distributions of oribatid mites among tolerance classes for drought are presented for the sites investigated that have a number of oribatid mites sufficient to make a pie-diagram possible (> 100 individuals). The difference between the forest sites (Fig. 3, a--c) and the low-input grasslands (Fig. 3, d-f) are the absence of the fraction of drought intolerant oribatid mites in the grasslands and the increase of the mesotolerant and tolerant fractions. '@ '@ a b c ~ W d e 4 - f - -? 1 avoiding 2 intolerant 3mesotolerant 4 tolerant Figure 3. Tolerance to drought of oribatid mites in old forest stands (a-c) and low-input grasslands (d-f). In high-input grasslands too few oribatid mites were present to make pie-diagrams. Tolerance classes are: 1, avoiding drought (species less than 250 p.m); 2, intolerant to drought (survival fraction of <33% after 48 hours exposure to 70% relative humidity); 3, mesotolerant to drought (survival fraction of 33-67%) and 4, tolerant to drought (survival fraction >67%) (Siepel, unpublished data).

8 258 Siepel Discussion In addition to the decrease in the number of species in the sequence: old forest stands, low-input grasslands, high-input grasslands, a number of changes in life-history tactics, feeding guilds and tolerance to drought has been shown. The task now is to identify the filters in the decline of the number of species, or to explain what the shifts in fractions of tactics, guilds and tolerances mean. The lower number of microarthropod species in the low-input grasslands compared with the old forest stands may be explained by the loss of drought intolerant species. As these grasslands are cut once a year in June, the chance of drought in the litter layer is quite serious. However, it is not enough to explain a difference of, on average, 27 species, as only a small number of those is intolerant to drought. Also long living thelytokously reproducing species that are tolerant or mesotolerant to drought disappear (such as Platynothrus peltifer and Nothrus silvestris), as well as other thelytokously reproducing species. Thelytoky and longevity are life-history traits that presume temporal predictability, a condition met in forest soils (Bengtsson, 1994), but not in grassland soils with a cutting and fertilization regime. The presence of a large fraction of fungivorous browsers indicates a good, and maybe rather constant growth of fungi. In the low-input grassland sites the fungivores which are left are of the grazer type (herbofungivorous and fungivorous grazers), able to digest fungal cell-walls, and thus able to survive long periods on dead mycelium. These guilds are almost completely lost in the high-input grasslands, where these fungivores are replaced by browsers again, but now with a phoretic life-history tactic (compare Fig. 1, g-i with Fig. 2, g-i). The fungivorous browsers in the forest stands are not phoretic, as fractions of II, III, and IV in Fig. 1, a-c are much lower than the fraction of fungivorous browsers (l) in Fig. 2, a-c, The consequence of the loss of fungivorous grazers is a less effective decomposition of organic matter as fungivorous grazers stimulate microbial activity and fungivorous browsers inhibit it (Siepel and Maaskamp, 1994), but that may be no problem in a currently high-input grassland. Restoration of such a site to more natural grasslands may be a problem because of the limited dispersal capacities of the fungivorous grazers that are needed. Abandoned high-input agricultural sites still have a lack of fungivorous grazers after twenty years of nature management, and maybe consequently a thick litter layer and a felting grasscover with very few plant species (Siepel, 1992). The mieroarthropod community of high-input grasslands consists of very opportunistic species with sexual reproduction and good dispersal capacities. The very few exceptions with thelytokous reproduction show a revival when the environment is made predictable again, but now with the high concentration of a persistent pesticide. The few individuals, by chance, able to handle or to avoid the pollutant found new populations that are able to grow to high densities (Table 1 ), maybe also because of the very low fraction of predators (Fig. 2, j). Summarizing, we may conclude that biodiversity of soil microarthropods is declining in the sequence: old forest stand, low-input grassland, high-input grassland. Within the high-input grasslands genetic diversity seems to decrease in relation to the application of a persistent pesticide. The pattern of decline is not random, as we found clear effects in shifts of life-history distributions in the community, as well as changes in feeding guild distributions and the disappearance of microarthropods intolerant to drought. Identification of the filters of biodiversity is a first step in its conservation. For conservation of soil microarthropods, conservation of virgin forests seems to be most important of all. In

9 Biodiversity of soil microarthropods 259 The Netherlands this part of nature has been lost already and none can tell how many microarthropod species have been lost in the step between virgin forests in an Atlantic climate and the old forest stands in this study. Acknowledgements My colleagues at the Institute are acknowledged for their participation in the discussion on this subject, which made the overwhelming complexity of biodiversity tractable. Ruut Wegman is acknowledged for preparing the Figures. References Anderson, J.M. (1975) The enigma of soil animal species diversity. In: Progress in Soil Zoology (J. Vanek, ed.) pp The Hague: Junk BV. Bengtsson, J. (1994) Temporal predictability in forest soil communities. J. Anim. Ecol. 63, Crossley, D.A. Jr, Mueller, B.R. and Perdue, J.C. (1992) Biodiversity of microarthropods in agricultural soils: relations to processes. Agricult. Ecosyst. Env. 40, Grandjean, F. (1941) Statistique sexuelle et parth6nogenese chez les Oribates (Acariens). Compte rendu hebdomadaire Sdance Acad~rnie Scientifique Paris 212, Hengeveld, R. (1994) Biodiversity - the diversification of life in a non-equilibrium world. Biodiver. Let. 2, Houte de Lange, S.M. ten (1977) Rapport van het Veluwe-onderzoek: een onderzoek van natuur, landschap en cultuurhistorie ten behoeve van de ruimtelijke ordening en het recreatiebeleid. Wageningen: Pudoc. Karg, W. (1971) Acari (Acarina), Milben Unterordnung Anactinochaeta (Parasitiformes), Die freilebenden Gamasina (Gamasides), Raubmilben. Die Tierwelt Deutschlands 59, Jena: Gustav Fischer Verlag. Karppinen, E. (1958) 13ber die Oribatiden (Acar.) der finnischen WaldbSden. Ann. Zool. Soc. Vanamo 19, Krczal, H. (1959) Systematiek und Okologie der Pyemotiden. Beitriige zur Systematik und Okologie mitteleuropaischer Acarina 1, Abschnitt 3, Lindquist, E.E. (1986) The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetic, and systematic revision, with a reclassification of family-group taxa in the Heterostigmata. Mem. Entomol. Soc. Canada 136, Martijn, A., Bakker, H. and Schreuder, R.H. (1993) Soil persistence of DDT, Dieldrin, and Lindane over a long period. Bull. Environm. Cont. Toxicol. 51, Moritz, M. (1965) Untersuchungen tiber den EinfluB von KahlschlagmaBnahmen auf die Zusammensetzung von Hornmilbengemeinschaften (Acari: Oribatei) norddeutscher Laubund Kiefernmischw~ilder. Pedobiologia 5, Petersen, H. (1971) Parthenogenesis in two species of Collembola: Tullbergia krausbaueri (Boerner) and Isotoma notabilis (Schaeffer). Rev. d'l~col. Biol. Sol 8, Siepel, H. (1992) Recovering of natural processes in abandoned agricultural areas: decomposition of organic matter. In: Proceedings of the 4th European Congress of Entomology (L. Zombori and L. Peregovits, eds) pp Budapest. Siepel, H. (1994) Life-history tactics of soil microarthropods. Biol. Fertil. Soils 18, Siepel, H. (1995) Applications of microarthropod life-history tactics in nature management and ecotoxicology. Biol. Fertil. Soils 19, Siepel, H. and van de Bund, C.F. (1988) The influence of management practices on the microarthropod community of grassland. Pedobiologia 31,

10 260 Siepel Siepel, H. and Maaskamp, F. (1994) Mites of different feeding guilds affect decomposition of organic matter. Soil Biol. Biochern. 26, Siepel, H. and de Ruiter-Dijkman, E.M. (1993) Feeding guilds of oribatid mites based on carbohydrase enzyme activities. Soil Biol. Biochem. 25, Soil Survey Staff (1975) Soil Taxonomy. A basic system of soil classification for making and interpreting soil surveys. Agriculture Handbook 436. Washington: Soil Conservation Service. US Department of Agriculture. Taberly, G. (1987) Rechhrches sur la parth4nogenese th41ytoque de deux hspeces d'acariens oribates: Trhypochthonius tectorum (Berlese) et Platynothrus peltifer (Koch). I. Acarologia 28, Tischler, E. (1965) Agrar6kologie. Jena: Gustav Fischer Verlag. Walter, D.E.~ Hunt, H.W. and Elliom E.T. (1988) Guilds or functional groups? An analysis ol predatory arthropods from a shortgrass steppe soil. Pedobiologia 31, Woodring, J.P. and Cook, E.F. (1962) The biology of Ceratozetes cisalpinus Berlese, Scheloribates laevigatus Koch, and Oppia neerlandica Oudemans (Oribatei), with a description of all stages. Acarologia 4,