Variability of the Oribatida/Prostigmata ratio in altered patches of the coastal matorral of the transitional desert of Chile

 

Variabilidad del índice Oribatida/Prostigmata en parches alterados del matorral costero del desierto transicional de Chile

 

Jorge Cepeda-Pizarro^1*, Jaime Pizarro-Araya^1,2, Víctor Bravo^{1, 2}

¹ Laboratorio de Entomología Ecológica, Departamento de Biología, Facultad de Ciencias, Universidad de La Serena, Casilla 599, La Serena, Chile.* Corresponding author: jcepeda@userena.cl
² Instituto de Investigación Multidisciplinar en Ciencia y Tecnología, Universidad de La Serena, La Serena, Chile.

---

ABSTRACT

The objectives of this study were to document the variability of the Oribatida/Prostigmata mite relationship (O/P) in altered patches of coastal matorral of the transitional desert of Chile, and to explore its viability as an indicator of the effects of soil degradation and its rehabilitation with introduced species. We studied a transect that extended through three latitudinal sections of matorral. The landscape of these sections consisted of patches dominated by: a) original matorral in semi natural condition, b) severely degraded patches of matorral aforested with Acacia saligna (Labill.) H.L. Wendl. (Fabaceae), c) severely degraded patches of matorral aforested with Atriplex nummularia Lind. (Amaranthaceae), and d) patches severely degraded, without afforestation. Results from patches aforested with A. saligna were inconclusive. The lowest O/P mean was obtained from patches without afforestation. Higher scores resulted from patches with semi-natural matorral and those afforested with A. nummularia. These results suggest that the O / P ratio has the potential to be used as an indicator of rehabilitation of degraded soils subject to improvement efforts of their plant cover. The O/P ratio obtained in this study tended to be higher than that found in previous work conducted in arid ecosystems. This result is probably due to the fact that, following current taxonomic criteria, we excluded Endeostigmata from the Prostigmata-counts. Since some Endeostigmata families are fairly common and abundant in arid and semi-arid soils, their elimination reduced the magnitude of the denominator of the relationship. The current taxonomic situation of Acari obliges us to redefine its value as an indicator and to explore its validity in a broader set of situations.

Key words: soil mites, drylands, desertification, ecosystem rehabilitation, biotic indices.

---

RESUMEN

Los objetivos de este estudio fueron documentar la variabilidad de la relación Oribatida/Prostigmata (O/P) en parches alterados del matorral costero del desierto transicional de Chile y explorar su viabilidad como indicador de los efectos de la degradación del suelo y su rehabilitación con especies introducidas. Estudiamos un transecto que se extendió por tres secciones latitudinales de matorral. El paisaje de estas secciones estuvo compuesto por parches dominados por: a) matorral original en condición semi-natural, b)parches severamente degradados, aforestados con Acacia saligna (Labill.) H.L. Wendl. (Fabaceae), c)parches severamente degradados, aforestados con Atriplex nummularia Lind. (Amaranthaceae), y d) parches severamente degradados, sin aforestación. Los resultados provenientes de los parches aforestados con A. saligna fueron noconcluyentes. Los promedios O/P más bajos se obtuvieron de los parches sin aforestación. Promedios más altos resultaron de los parches con matorral en condición seminatural y aquellos aforestados con A. nummularia. Estos resultados sugieren que la proporción O/P tiene potencialidad para ser usada como indicador de rehabilitación de suelos degradados sujetos a esfuerzos de mejoramiento de su cubierta vegetal. La relación O/P obtenida en este estudio tendió a ser más alta que la encontrada en trabajos previos conducidos en ecosistemas áridos. Este resultado probablemente se deba al hecho que, siguiendo criterios taxonómicos más actuales, excluimos Endeostigmata de los recuentos de Prostigmata. Puesto que algunas familias de Endeostigmata son bastante comunes y abundantes en suelos áridos y semiáridos, su eliminación redujo la magnitud del denominador de la relación. La actual situación taxonómica de Acari nos obliga a redefinir su valor como indicador y explorar su validez en un conjunto más amplio de situaciones.

Palabra clave: ácaros edáficos, tierras secas, desertificación, rehabilitación del ecosistema, índices bióticos.

---

Introduction

Soil is one of the main components of terrestrial ecosystems, and much research is needed on the subject to support local sustainable development goals (Keesstra et al., 2016). In the Chilean case, vast areas of the coastal matorral of its transitional desert are affected by severe desertification (Gastó et al., 1990). Government programs to mitígate the effects of this phenomenon and to recover partially the ecosystem services have been launched since some decades. These actions have heavily rested on the introduction of plant species from arid regions at other latitudes (Alfaro, 2006). As of today, the effects of degradation and rehabilitation efforts are poorly understood, limiting application of effective restoration practices (Kelt & Meserve, 2016). One of the goals of ecological restoration is to improve soil productivity of degraded ecosystems. Soil productivity is a synergetic result of action of many interaction agents, among them its biota. Certain abundance patterns appear to exist between some elements of the soil biota and soil conditions (Nielsen et al., 2010). For instance, due to their abundance and responsivity to environmental factors, the abundance relationships of mite taxa have been proposed as potential indicators of soil conditions. One of these indices is the Oribatida/Prostigmata ratio (O/P ratio hereafter). The O/P ratio is supposedly indicative of soil's organic matter and moisture characteristics (Andrés & Mateos, 2006). The objectives of this work were (a) to document the variability of the O/P ratio under different patch-conditions found in the coastal matorral of the transitional desert of Chile, and b) to explore the feasibility of use as an indicator of soil biological condition, especially in relation to rehabilitation efforts.

Materials and Methods

Study Area

The study encompassed a coastal stretch of ~200 km of north-central Chile (Figure 1). The historical range of annual precipitation of the area shows a clear latitudinal gradient, with values ranging from 105 mm (northern margin) to 210 mm (southern margin) (Novoa & Villaseca, 1989). Nevertheless, this gradient was not clearly expressed during the study year (Meteorological Office of the Chilean Navy, unpublished data). Soils belong to the torripsamment-group, with isothermic and aridic (torric) regime (Casanova et al., 2009). Preliminary data show that soil texture ranges from sandy (93.9-96.2% of sand) to loamy-sand (68.9-74.2%). The range of SOM of soil surface (top 0.3 m) is low to medium (0.5 to 2.5%); N and P contents are low to very low; the K-level tends to be very high (>250 ppm). The study transect spanned three latitudinal sections of matorral (Luebert & Pliscoff, 2006; Gajardo, 1995). From north to south, they are named in this work as (1) low-shrub matorral (MEC hereafter), dominated by Oxalis gigantea-Heliotropium stenophyllum; (2) shrubby matorral (MEB), dominated by Bahia ambrosioides-Puya chilensis, and (3) sclerophyllous matorral (MEA), dominated by Peumus boldus-Schinus latifolious. Because the strong anthropic pressure affecting the area, well-conserved matorral is almost nonexistent, except in hard-to-reach gorges. Today, most landscape is made of seminatural patches of matorral (SNV patches hereafter); severely degraded patches, rehabilitated with Atriplex nummulariaLind. (Amaranthaceae), (ANU patches) or Acacia saligna (Labill.) H. L. Wendl. (Fabaceae) (ASA patches), and severely degraded patches (SDE patches), without rehabilitation efforts.

Figure 1. Geographic location of study sites. Latitudinal sections of matorral in the study stretch (30°06' S-31°56' S). A: low-shrub matorral; B: shrubby matorral; C: sclerophyllous matorral. Latitudinal sections of matorral after Gajardo (1995). Details of geographic locations of study sites and patch types are found in Table 1.

Mite Sampling and Processing

Sampling was conducted in early spring (October of 2012). In all the cases, the soil mites were captured from a composite sample made by combining four subsamples, making a total volume of ~0.8 L by composite sample. Each subsample was collected with a metal cylinder (0.05 m in diameter) that was introduced into the soil up to a depth of 0.20 m. The study of the VSN-patch was based on five composite samples obtained from underneath well-grown individuals of Peumus boldo Mol. (Monimiaceae) found in the sclerophyllous section of the study transect (Table 1). Each subsample was collected from the same individual, following a cardinal orientation. The samples for the study of the ANU-patch were obtained from a mature and well-established plantation (Table 1). In this case, five healthy and well-grown individuals separated at least 30 m from each other were selected. For each one of them, subsamples were collected following the cardinal points. The samples for the study of the ASA-patch were obtained from a mature and well-established plantation located in the sclerophyllous section of the study transect (Table 1). The five samples were selected following the sampling criteria described for the VSN-patch. The samples for the study of the DES-patch were obtained from sites representing the three latitudinal sections of matorral (Table 1). In this case, five 100-meter transects were established in each sampling site; the four subsamples were obtained from four cardinal points established from reference points located along the transect at 25-m intervals, with a minimum distance between opposite cardinal points of approximately 1 meter. This sampling effort yielded 15 composite samples for the SDE-patch. For comparative purposes, we considered five samples from a rainfed alfalfa crop found in the sclerophyllous section of the study transect (Table 1). The crop was rather light, with dominance of individuals of low growth. In this case, samples were collected according to the criteria used for the analysis of the DES-patch. Sampling was conducted in October (early spring for the area). In all cases, samples were taken between 9.00 a.m. and 12.00 p.m. Before sample collection, the litter deposited on the soil surface, if any, was removed. Once collected, we placed the samples in plastic bags, which were sealed and stored in refrigerated containers for transportation. Once in the lab, the samples were opened and left open for 24 hours for the specimens contained in them to acclimate to lab conditions. Twice during the first day, the soil was moistened with drinking water that had been previously boiled and left to cool. The water was applied with a manual gardening sprinkler. Every time, the soil was removed to facilitate moistening. After 24 hours, the samples were placed in soil-fauna extractors (Cepeda-Pizarro et al. 1996). The extractors remained in operation for 72 continuous hours. The mites were collected in plastic vials containing a picric acid solution (3%). Once sorted out, the specimens were preserved in an ethanol-glycerin solution (5:1) until processing and counting. The taxonomic identification followed Lindquist et al. (2009). Differences among patch-types were tested with ANOVA (one-way). To carry out the test the raw data were arcsine transformed. The statistical analyses were performed in Statistix, version 10 (Analytical Software, 2013).

Table 1. Geographic location of study patch types in a coastal latitudinal stretch (30°06' S to 31°56' S) of the transitional desert of Chile.

*Code: VSN: seminatural patch type; SDE: heavily degraded patch type; ASA: Acacia saligna aforested patch type; ANU: Atriplex nummularia aforested patch type; PRA: rainfed alfalfa crop; PLV (latitudinal section of matorral): MEA: sclerophyllous matorral; MEC: low-shrub matorral; MEB: shrubby matorral. PLV named after Gajardo (1995).

Results and Discussion

We captured 1803 specimens in total, most of them in the suborders Oribatida (63.7% of total captures), followed by Astigmata (15.5%), Prostigmata (13.5%), and Mesostigmata (7.3%). The patch-types that most contributed to total capture were the acacia-patch (40.6%) and the matorral in semi natural condition (36.3%), both stands located in the sclerophyllous fringe of the study transect (Table 1). The nummularia-patch (low-shrub matorral, Table 1) contributed with 9.0%. In turn, the rainfed alfalfa crop (sclerophyllous section of matorral) provided the 4.3%. The lowest contribution came from the highly degraded patches (SDE-patches); by latitudinal section of matorral, the SDE-patches provided a mean of 3.3%. Irrespectively these numbers, the mean O/P ratio followed a different trend, ranging from 1.8 (SDE-patch, low-shrub matorral) to 6.1 (ANU-patch, low-shrub matorral) (Table 2). The mean-ratios found in this work for the SDE-patch and the rainfed alfalfa crop are within the limits reported from other arid sites (e.g., Noble et al., 1996; Di Castri & Vitali-Di Castri, 1981). This low value probably reflects the mite fauna's level of exposure to prevailing environmental factors in the study area (e.g., unfavorable moisture conditions, strong solar radiation, and intense sea winds, especially during the dry season of the year). Although we did not detect significant differences among latitudinal sections of matorral (Table 3, comparison 1), the mean ratio of the SDE-patch showed an apparently gradual increase in the north-to-south direction suggesting a trend of better soil conditions towards central Chile, as advanced by Salazar & Sáiz (1983-1985).

Table 2. O/P mean ratio ± se (CV) by patch type*.

SDE1: samples from the low-shrub matorral (MEC section of latitudinal transect of vegetation PLV); SDE2: samples from the shrubby matorral (MEB section of PLV); SDE3: samples from the sclerophyllous matorral (MEA section of PLV). Other codes as in Table 1.

Table 3. Effect of patch type on the O/P ratio.

* (1) comparisons among MEC, MEB, and MEA-sites; (2) comparison within MEC-sites; (3) comparison within MEA-sites; (4) comparisons among all sites. See Table 1 for PLV-code. The ANOVA-test was conducted on arcsine transformed data.

As expected, soil covered by litter provided higher mean ratios as compared to the rainfed alfalfa crop and the heavily degraded matorral (Table 3, comparisons 2 through 4). High mean ratios indicate better moisture and organic matter conditions (Nielsen et al., 2010). Among the littered-soil, we found the highest mean ratios in the nummularia-patch (6.1) and in the matorral in semi natural condition (5.3). The relatively high mean ratio provided by the nummularia-patch was an unexpected result. The nummularia-revegetation in the area apparently do not promote faunal colonization (Kelt & Meserve, 2016). In the case of soil biota, salinization and oxalate concentration induced by nummularia-litter decomposition (Zohra et al., 2014), may prevent colonization after revegetation. This change in chemical conditions of soil surface can explain the low total abundance of mites we found in this patch-type (9.0% of total capture). Nevertheless, there was a clear numerical dominance of Oribatida (7.9% of total capture) over Prostigmata (0.7%). As we registered in the field, there was a well-decomposed and thick layer of litter beneath the nummularia-plants. These litter characteristics are probably due to the age of study stand (> 30 years). In an area where the sea fog is an important source of water, we believe this layer protect the soil underneath the plant from rapid desiccation, along with providing nutrients for microbial growth. Former work in the area has documented that atriplex-species induce higher contents of nutrients (e.g., P y N) under the plants, as well as salinization (Lailhacar et al., 1983). Due to state of knowledge, we did not perform a finer taxonomic analysis to pay attention on the selective effect of salinization. We hypothesized that the mite assemblage is made up by a few numerically dominant species, selected to live in a saline environment. Although the acacia-patches provided the highest number of mites (40.6% of total capture), the mean O/P ratio of the acacia-patch was the lowest one among the littered-patches (Table 3). This value can be related to the elevated levels of cellulose, lignin and tannins that leaves of A. saligna contain, all of which prevent high decay rates (Ahmed et al., 2015), and to the relatively young age of the plantation (< 15 years). In this case, we registered a thin layer of non-decomposed litter under the trees or not layer at all.

Literature reports that the O/P ratio tends to be lower in soils of arid environments as compared to moist environments. In Chile, for instance, reported values range from 0.4 (arid north) to above 10.0 (moist south) (Covarrubias & Contreras, 1999; Berríos, 2002). Nevertheless, when examining this ratio at a smaller spatial scale (e.g., microhabitat), this trend may be observed altered (Noble et al., 1996). These results are interpreted as an expression of the diversity of microhabitats found in desert environments.

Although there is some criticism to the approach (Kelt & Meserve, 2016), most of the campaigns addressed to recover ecosystem services provided by the coastal transitional desert of Chile, have been based on the introduction of either exotic or invasive species (Latorre, 1999). Soil biota can change after these efforts, affecting ecosystem processes (Belnap et al., 2005). These effects remain unknown so far in Chile. Consequently, further and finer studies are required to unveil the process of replacement of original soil biota. Based on this knowledge, it is essential to develop low-cost and easy-to-apply strategies that allow monitoring ecosystem changes with a reasonable amount of effort. Based on the results found in this study, we believe that the Oribatida/Prostigmata ratio meet these requirements. However, attention must be paid that literature shows this ratio varies widely. Part of this variability is due to changes in the classification criteria of Acari. In fact, whereas Krantz's classification (1978) includes Endeostigmata in the SubOrder Prostigmata, it is excluded from Lindquist et aUs classification (2009). Some families of Endeostigmata (e. g., Nanorchestidae) are quite common in arid soils, being responsible for the low value reported in earlier works (e.g., Cepeda-Pizarro & Whitford, 1990). It is clear that more taxonomic stability and precision regarding the field biology of the mite assemblages are needed for a validation of this index.

Conclusion

In general, the soil mite was found to be relatively impoverished in the study area. The O/P ratio proved its potential as a suited indicator of soil degradation and rehabilitation processes. In fact, its value in denuded patches was lower than the ratios found in the semi natural patches of matorral and those afforested with Atriplex nummularia. The difference observed between the denuded patches and the A. saligna-afforested patches was inconclusive. Probably, the older age of the A. nummularia-patches as compared to the A. saligna-patches and its lower levels of recalcitrant chemicals are responsible of the difference in the O/P ratio between both patch-types. Nevertheless, the O/P ratio needs to be validated in a wider set of situations to be used as biotic index of soil rehabilitation campaigns conducted in the transitional desert of Chile, especially under the new taxonomical considerations that rule present-day mite's classification. It is also clear that knowledge on field biology and the environmental context of the mite assemblage need also to be improved.

Acknowledgment

Financial support for this study was provided by the Research Office of University of La Serena (La Serena, Chile), Res. Proj. 14121 to Jorge Cepeda-Pizarro. The authors wish to thank H. Vásquez C., A. Levicán D., and Ariane González V. for field and laboratory assistance, and R. Castillo H. for paper translation. We extend our thanks to two anonymous reviewers.

Literature Cited

Ahmed, M.H.; Elghandour, M.M.Y.; Salem, A.Z.M.; Zeweil, H.S.; Kholif, A.E.; Klieve, A.V.; Abdelrassol, A.M.A. 2015. Influence of Trichoderma reesei or Saccharomyces cerevisiae on performance, ruminal fermentation, carcass characteristics and blood biochemistry of lambs fed Atriplex nummularia and Acacia saligna mixture. Livestock Science, 180: 90-97.

Alfaro, C.W. 2006. Implementación en Chile de la Convención de Naciones Unidas contra la Desertificación en los países afectados por sequía grave o desertificación, en particular África. Tercer Informe Nacional. Oficina de Coordinación Nacional PANCCD-Chile. Punto Focal Nacional en Chile. Departamento de Manejo y Desarrollo Forestal. Gerencia de Desarrollo y Fomento Forestal. Corporación Nacional Forestal (CONAF). Ministerio de Agricultura. Santiago, Chile.

Analytical Software. 2013. Statistix 10. Analytical Software. Tallahassee, Florida, USA.

Andrés, P.; Mateos, E. 2006. Soil mesofaunal responses to post mining restoration treatments. Applied Soil Ecology, 33: 67-78.

Belnap, J.; Phillips, S.L.; Sherrod, S.K.; Moldenke, A. 2005. Soil biota can change after exotic plant invasion: does this affect ecosystem processes? Ecology, 86: 3007-3017.

Berríos, P. 2002. Artrópodos asociados a suelo de renovales de Notophagus obliqua (Mirb.) Oersted (Fagaceae) en la zona costera de la VIII Región. Gayana, 66: 1-9.

Casanova, M.; Seguel, O.; Luzio, W. 2009. Suelos de la Zona Árida y Semiárida (desde 29° LS hasta 32° LS). En Suelos de Chile, Luzio, W. (ed.). Universidad de Chile, Santiago, Chile, pp. 81-123.

Cepeda-Pizarro, J.; Gutiérrez, J.R.; Valderrama, L.; Vásquez, H. 1996. Phenology of the edaphic microarthropods in a Chilean coastal desert site and their response to water and nutrient amendments in the soil. Pedobiologia, 40: 352-363.

Cepeda-Pizarro, J.; Whitford, W.G. 1990. Microartrópodos edáficos del desierto Chihuahuense, al norte de México. Folia Entomológica Mexicana, 78: 257-272.

Covarrubias, R.; Contreras, A. 1999. Efecto de manejos forestales del bosque siempre verde chilote sobre los microartrópodos del suelo. Bosque, 20: 25-38.

Di Castri, F.; Vitali-Di Castri, V. 1981. Soil fauna of mediterranean-climate regions. In: Di Castri, F., Goodall, D.W. and Specht, R.L. (eds.) Mediterranean-type shrublands, Series Ecosystems of the World. Vol. 11. Elsevier Scientific Publications Company. New York. Us. pp. 1-52.

Gajardo, R. 1995. La vegetación natural de Chile. 2^a edición. Colección Imagen de Chile. Editorial Universitaria. Santiago, Chile. 165 p.

Gastó, C.J.; Contreras, D.; Cosio, F.; Demanet, R. 1990. Degradación y rehabilitación de la zona mediterránea de Chile. Terra Arida, 8: 171-220.

Keesstra, S.D.; Bouma, J.; Wallinga, J.; Tittonell, P.; Smith, P.; Cerda, A.; Montanarella, L.; Quinton, J.N.; Pachepsky, Y.; van der Putten, W.H.; Bardgett, R.D.; Moolenaar, S.; Mol, G.; Jansen, B. 2016. The significance of soils and soil science towards realization of the United Nations Sustainable Development Goals. Soil, 2: 111-128.

Kelt, D.A.; Meserve, P.L. 2016. To what extent can and should revegetation serve as restoration?. Restoration Ecology, 24: 441-448.

Krantz, G.W. 1978. A manual of Acarology, Oregon State University Book Stores Inc., Corvallis, Oregon, USA.

Lailhacar, K.S.; Carrasco R.A.; Badilla, S. 1983. Efecto del arbusto forrajero Atriplex repanda Phil. en algunas propiedades del suelo superficial. Terra Arida, 2: 257-284.

Latorre A.J. 1999. Reforesatation of arid and semi-arid zones in Chile. Agriculture, Ecosystems & Environment, 33: 111-127.

Lindquist, E.E.; Krantz, G.W.; Walter, D.E. 2009. Classification. In: A manual of Acarology, Krantz G.W., Walter D.E. (eds.) Third Edition. Texas Tech University Press. Lubbock, Texas, USA. pp. 97-103.

Luebert, F.; Pliscoff, P. 2006. Sinopsis bioclimática y vegetacional de Chile. Editorial Universitaria. Santiago, Chile. 316p.

Nielsen, U.N.; Osler, G.H.; Campbell, C.D.; Burslem, D.F.R.P.; van der Wal, R. 2010. The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. Journal of Biogeography, 37: 1317-1328.

Noble, J.C.; Whitford, W.G.; Kaliszweski, M. 1996. Soil and litter microarthropod from two contrasting ecosystem in semi-arid eastern Australia. Journal of Arid Environments, 32: 329-346.

Novoa, R.; Villaseca, S. 1989. (eds.) Mapa agroclimático de Chile. Instituto de Investigaciones Agropecuarias. Ministerio de Agricultura. Santiago, Chile. 221 p.

Pérez, C.; González, J. 2001. Diagnóstico sobre el estado de degradación del recurso suelo en el país. Instituto de Investigaciones Agropecuarias-CONAMA. Ministerio de Agricultura, Gobierno de Chile, Santiago, Chile. 196p.

Salazar, A.; Saiz, F. 1983-1985. Efecto de Acacia caven (Mol.) Hook et Arn. sobre la acarofauna edáfica. Anales del Museo de Historia Natural, 16: 55-70.

Zohra, Y.F.; Labani, A.; Terras, M.; Anteur, D.; Adda-Hanifi, N.N.; Kerache, G.; Hadouche, M.I. 2014. Study of the impact of three species of Atriplex (Atriplex halimus, Atriplex nummularia and Atriplex canescens) on the soil physico-chemical parameters in the steppe zone; case of the south west of Algeria. European Scientific Journal, 10: 1857-7881.

---

Fecha de Recepción: 19 Agosto, 2016. Fecha de Aceptación: 10 Mayo, 2017.