Applied Soil Ecology 58 (2012) 66–77

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Applied Soil Ecology

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Nematodes as an indicator of plant–soil interactions associated with desertiﬁcation

a,∗ b c c

Jeremy R. Klass , Debra P.C. Peters , Jacqueline M. Trojan , Stephen H. Thomas

New Mexico State University, Plant and Environmental Science, Las Cruces, NM 88003-8003, USA

USDA-ARS Jornada Experimental Range and Jornada Basin LTER, Las Cruces, NM 88003-8003, USA

New Mexico State University, Entomology, Plant Pathology, and Weed Science, Las Cruces, NM 88003-8003, USA

a r t i c l e i n f o a b s t r a c t

Article history: Conversion of perennial grasslands to shrublands is a desertiﬁcation process that is important globally.

Received 5 October 2011

Changes in aboveground ecosystem properties with this conversion have been well-documented, but

Received in revised form 14 February 2012

little is known about how belowground communities are affected, yet these communities may be impor-

Accepted 8 March 2012

tant drivers of desertiﬁcation as well as constraints on the reversal of this state change. We examined

nematode community structure and feeding as a proxy for soil biotic change across a desertiﬁcation

Keywords:

gradient in southern NM, USA. We had two objectives: (1) to compare nematode trophic structure and

Semi-arid grasslands

species diversity within vegetation states representing different stages of desertiﬁcation, and (2) to com-

Nematode communities

pare nematode community structure between bare and vegetated patches that may be connected via a

Nematode diversity

Connectivity matrix of endophytic fungi and soil biotic crusts. The gradient included a perennial grassland dominated

Bouteloua eriopoda by Bouteloua eriopoda, the historic dominant in the Chihuahuan Desert, a duneland dominated by the

Prosopis glandulosa shrub, Prosopis glandulosa, and the ecotone between them. We also sampled a relatively undisturbed,

ungrazed B. eriopoda grassland at a nearby site to serve as an end member of our gradient. Nematode

communities were sampled using soil cores to depth of 50 cm at each location in 2009 and 2010. Results

showed that grasslands and mesquite dunelands had different trophic groupings and herbivorous nema-

tode communities with lower species diversity and evenness compared with the ecotone. Nematode

trophic structure and herbivore communities were signiﬁcantly different in all vegetation states with

the highest observed diversity in the undisturbed, ungrazed B. eriopoda grassland in 2010. Vegetated and

bare ground patches within the two grassland sites had similar herbivore communities, especially species

from the family Tylenchinae. However, the mesquite duneland showed the lowest sampled diversity of

all sites, but had signiﬁcantly larger nematode abundances in vegetated dunes than interdune areas that

are void of vegetation and soil biotic crusts where bacteriovores dominated. Decreased nematode trophic

structure and species diversity in the Jornada black grama grassland samples compared with the undis-

turbed grassland illustrate the effect of desertiﬁcation on the soil biotic community. Our results show

that nematodes can be used to identify changes in belowground community structure based on trophic

interactions. Large-scale disturbances like desertiﬁcation can have consequences on the diversity and

soil biotic functioning at ﬁner spatial scales.

1. Introduction and losses in soil nutrients that favor woody plants (Schlesinger

et al., 1990; Archer, 1994; Abrahams et al., 1995; Parsons et al.,

Desertiﬁcation of arid lands is a global problem, with nearly 1997; Whisenant, 1999; Wainwright et al., 2000; Peters, 2002a,b).

40% of the world’s land area either already converted or suscep- Examining effects of drivers (e.g., multi-year drought, livestock

tible to a state change from productive grasslands to degraded overgrazing) of state changes on landscape-scale patterns often

shrublands or woodlands (Reynolds and Stafford Smith, 2002). focus on vegetation responses; much less is known about changes

These ‘state’ changes are difﬁcult to restore because of the loss of in belowground communities that can inﬂuence vegetation

herbaceous productivity, grass propagules, and modiﬁcations in dynamics. However, shifts in belowground community structure

soil surface properties that result in increases in runoff and erosion associated with desertiﬁcation may provide a constraint on the

ability of grasses to recover if soil biota critical to grass success are

missing from the shrubland. Because arid ecosystems consist of a

∗ mosaic of grass or shrub plants and bare soil interspaces (i.e., gaps),

Corresponding author. Tel.: +1 575 571 6107; fax: +1 575 646 6041.

differences in soil biota between these two microhabitats may

E-mail address: [email protected] (J.R. Klass).

J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77 67

have important consequences for grass recovery. Our goal was to 1999; Ritz and Trudgill, 1999; Bongers and Ferris, 1999; Ferris et al.,

determine how soil biota differs across a grassland-to-shrubland 2001; Neher, 2010).

gradient of increasing woody plant abundance. This study relies on the quantiﬁcation of nematodes with spe-

The composition of soil organisms (e.g., nematodes, bacteria, ciﬁc, morphologically distinguishable feeding behaviors as a proxy

fungi, etc.) determines the inﬂuence of the soil microbial commu- for characterizing changes in soil biota. We addressed the questions

nity on plant assemblages, in general (Ogle and Reynolds, 2004; to represent two spatial scales across a desertiﬁcation gradient:

Reynolds et al., 2004; Collins et al., 2008). Soil biota can affect (1) how do nematode communities, and presumably the soil biotic

the establishment and abundance of individual plant species with consortia of vegetation states (black grama grasslands vs. mesquite

consequences for functional group and species diversity (van der shrublands), change? and (2) how do nematode communities differ

Putten et al., 1993; Molofsky, 1994; Bever et al., 1997; Mills between bare soil gaps and vegetated patches within each domi-

and Bever, 1998; Klironomos et al., 2000; Molofsky et al., 2001; nant vegetation type?

O’Hanlon-Manners and Kotanen, 2004; Reinhart et al., 2003, 2005).

A disruption or disturbance to soil biotic consortia can play an

integral role in the dynamics of a system, and may be responsi- 2. Methods

ble for either promoting shrub invasion or limiting grass recovery

(Wardle et al., 2004). In some cases, interactions between soil biota 2.1. Study site

and plants can generate feedback mechanisms among soil biotic

crusts, fungi, and plants (Belnap, 1996; Collins et al., 2008; Green The study was conducted at the USDA-ARS Jornada Experimen-

et al., 2008; Lucero et al., 2008; Porras-Alfaro et al., 2007, 2011; tal Range (JER) and Jornada Basin Long-Term Ecological Research

◦ ◦

Porra-Alfaro et al., 2008). Soil biotic crusts serve as an interface Site in southern New Mexico, USA (32 37 N, 106 40 W, and 1260 m

between the soil and atmosphere capable of ﬁxing N and C while a.s.l.). The JER is a 100,000 ha research site located within the north-

affecting the abundance, diversity, and successional maturity of ern extent of the Chihuahuan Desert. Long-term (1915–2009) mean

other soil biota (Evans and Belnap, 1999; Belnap, 2003; Garcia- annual rainfall is 246 mm that is highly variable from year to year

Pichel et al., 2003; Darby et al., 2006). Dark septate fungi (DSF) with more than half of the precipitation occurring between July and

◦

are the dominant colonizers of many native plants as well as B. October. Mean monthly average temperatures peak in June (26 C)

◦

eriopoda in the arid southwest that have the ability to manage and are lowest in January (4 C). Upland grasslands on sandy soils

and regulate carbon in plant communities, aid in nutrient acqui- with a petrocalcic horizon at the JER are dominated by black grama

sition and allocation, and provide increased drought tolerance to (B. eriopoda) with mesa dropseed (Sporobolus ﬂexuosus) and vari-

hosts (Barrow, 1997; Barrow et al., 2004; Lucero et al., 2006; Porra- ous three-awn species (Aristida spp.) as sub-dominate species. Over

Alfaro et al., 2008) The extension of fungal symbionts of B. eriopoda the past century, large areas of the upland grasslands have con-

leads us to expect that increased connectivity of vegetated patches verted to shrublands dominated by honey mesquite (P. glandulosa)

in grasslands harbor soil biotic communities linking vegetation (Fig. 1).

and soils biotic crusts that occupy bare ground patches. Shrub Sample locations were selected to represent both remnant

encroachment and increases in bare ground gaps that perpetu- black grama patches and historic areas that were previously grass-

ate erosion/deposition processes causes vegetative production and lands and are currently dominated by mesquite. The black grama

decomposition of organic matter to be much more heterogeneous and mesquite sites are the two end members of a desertiﬁcation

that can have long term effects on nutrient availability and relegate gradient, with a mixture of grasses and shrubs in the ecotone

soil biotic communities to isolated vegetated patches (Schlesinger (Bestelmeyer et al., 2006). The ecotone sampling area represents

et al., 1990; Kéﬁ et al., 2007; Ravi et al., 2007; Scanlon et al., 2007). the transition zone between the two end members as part of

The Chihuahuan Desert of North America provides an oppor- the desertiﬁcation gradient. These transition zones, or ecotones,

tunity to evaluate these processes and feedbacks. The vegetation present optimal conditions because they are areas that have a

on sandy soils consists of perennial grasses, primarily black grama high probability of response and are likely to experience thresh-

(Bouteloua eriopoda) and the shrub, honey mesquite (Prosopis old behavior, possess key processes that must be manipulated or

glandulosa) that occur at variable proportions of cover across a maintained in order to uphold current conditions or to reverse a

landscape, yet total vegetation cover is similar. A key system prop- current undesirable trend, and provide early warning indicators

erty that differentiates grasslands from shrublands is the spatial that can be used to monitor and evaluate changes in critical pro-

distribution and density of plants and their associated bare soil cesses (Peters et al., 2006). Because ecotones are deﬁned by speciﬁc

interspaces (gaps) (Herrick et al., 2005; Okin et al., 2006). The characteristics, they allow for the evaluation of the impact of deser-

low diversity of soil organisms compared with mesic systems is tiﬁcation on a landscape scale interacting with ﬁne-scale soil biotic

most likely due to species operating close to their physiological communities speciﬁc to B. eriopoda and P. glandulosa.

tolerance limits in the hot and dry abiotic environment (Whitford, Soils on the Jornada vary in texture from sandy loams to loamy

1996). Therefore, the limited functional redundancy of soil biota sands with an indurated calcium carbonate layer at 15 to >50 cm

in arid systems increases the susceptibility of soil biotic commu- depths (Hochstrasser et al., 2002). All geomorphic descriptions for

nities to disturbances that can lead to profound impacts upon the Jornada Basin follow Monger et al. (2006). Sample locations all

ecosystem processes (Wall and Virginia, 1999). A study of plant occur on the same ancestral Rio Grande alluvium parent material

parasitic nematodes revealed less herbivory within a duneland site of the Camp Rice Formation, Fluvial Facies. These strongly devel-

compared with grassland sites that was suggested to aid in estab- oped soils with thick petrocalcic horizons are components of the

lishment of mesquite (Wall and Virginia, 1999). La Mesa surface where wind erosion has been the main source of

Because of the ubiquity and abundance of nematodes and the quartzose sand accumulated on down-wind piedmont slopes and

trophic speciﬁcity they exhibit, nematode community structure bedrock areas.

offers an efﬁcient tool to assess soil biological function and food Nematode samples were also collected from Otero Mesa on

web quality (Bongers and Ferris, 1999). Speciﬁc nematode genera June 11, 2010 to be used as a complement to the desertiﬁca-

are active within each heterotrophic food web level and can be tion gradient on the JER. Otero Mesa represents a reference site

grouped by functional guilds whose members respond similarly of intact, relatively undisturbed B. eriopoda grasslands. This Chi-

◦ ◦

to food web enrichment and to environmental perturbation and huahuan Desert site (32 30 N, 105 47 W) has the largest intact,

recovery (Yeates et al., 1993; Bongers and Bongers, 1998; Bongers, public desert grassland in America (485,622 ha). Roughly half of

68 J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77

Fig. 1. Progression of shrub encroachment through time at the Jornada LTER site, Dona˜ Ana County, NM. Vegetation delimited is all grass species and all woody shrub species

on the Jornada through time; courtesy of David Rachal. Created with GIS software package and datalayers obtained from Gibbens et al. (2005).

Otero Mesa is grassland, dominated by two species that occur on activity would be kept to a minimum. Each soil sample consisted

upland shallow soils, B. eriopoda and Bouteloua gracilis (blue grama). of three cores randomly collected using a 7 cm diameter auger to

P. glandulosa is virtually absent from the site and minimal wild a depth of approximately 50 cm, and composited in sterile plastic

and domesticated large animal grazing occurs. Mean annual pre- bags. A total soil volume of 1.1 l was collected from each sampling

cipitation is 255 mm/year with the majority occurring during the location within each vegetation site for nematode extraction, and

warm season (May–October). Soils of the sampled area are pre- to determine percentage soil moisture concentration at the time

dominantly silty, shallow calcareous soils derived from Paleozoic of sampling. Soil moisture values are not reported because values

limestone that also contains an indurated calcium carbonate layer. did not differ signiﬁcantly among soil sampling sites or dates, and

The mean annual precipitation is 255 mm/year with the majority nematode numbers were not correlated to soil moisture, similar

occurring during the warm season (May–October). to previous studies (Freckman and Virginia, 1989). Grassland soil

samples were collected in three microsites: (1) beneath a black

2.2. Soil sampling and nematode extraction grama patch that included the rooting zone; (2) from areas void

of aboveground vegetation that had visible soils crusts (identiﬁed

Sampling at both sites occurred in two years during the dry sea- as either of two cyannolichens, the rugose soil crust Peltula richard-

son (2009 June 11 2009; 2010 May 27) to ensure that soil biotic sii or Collema sp.); and (3) from areas between vegetated patches

J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77 69

Table 1

Soil sampling regime from both the Jornada and Otero Mesa sites indicating sample year, within site soil sample location, soil sampling scheme, and soil sampling strategy.

Number in parentheses indicates the number of samples sampled in a giver year, numbers in sample location area breakdown of the total number of samples from 2009;

2010 sampling years.

Site Jornada Otero Mesa

Sample year 2009 (33)/2010 (50) 2010 (15)

Sample location Grassland (12; 15)/ecotone (9; 15)/duneland (12; 20) Undisturbed grassland (15)

Within site sample scheme Bare ground/vegetated patch/crust/dune/interdune Bare ground/vegetated patch/crust

Soil sampling strategies and analysis Nematode extraction and enumeration, species diversity Nematode extraction and enumeration, species diversity

and evenness, FB, HB, HT ratio analysis, connectivity and evenness, FB, HB, HT ratio analysis, connectivity

analysis. analysis.

that had little visual evidence of soil biotic crusts. Ecotone soil sam- species as well as rescaled each signiﬁcant axes’ with 26 segments

ples were taken in areas where black grama and mesquite co-occur (McCune and Mefford, 2006). To determine the signiﬁcance of the

at varying amounts of vegetative cover. Soil samples in the ecotone nematode community loadings on individual axes derived from

sites were collected from three microsites: (1) directly beneath a each DCA, a multiresponse permutation procedure was applied

mesquite shrub canopy, (2) within a patch of co-occurring black (MRPP) using Euclidean (Pythagorean) as the distance measure and

grama, and (3) from bare ground between a sampled black grama c(I) = n(I)/sum(n(I)) as the weighting option (PC-ORD Version 5.32).

patch and the nearest neighboring patch. Dune sampling mimicked The MRPP is a non-parametric procedure for testing the hypothesis

a previously conducted pilot project that examined dune archi- that no difference exists between two or more groups of entities,

tecture and identiﬁed which aspect of the dune would yield the and provides a signiﬁcance test of DCA scores for each axis. The

greatest number of nematodes per sample. Based on the pilot-study procedure is therefore not held to the assumptions of multivari-

data, soil samples were taken from the top, the north and south ate normality and homogeneity of variance that seldom apply to

faces of each dune as well as an interdune sample located on the ecological data (Cai, 2006; McCune and Mefford, 2006). The MRPP

windward, southern facing side of each dune sampled. All soil sam- analyses also allow for pairwise comparisons that can be used to

ples were placed in a cooler to regulate soil temperatures during compare nematode community groupings among the different veg-

transport to the lab (Table 1). etation sites. DCA rescales and detrends the original axes, therefore

the traditional interpretation of eigenvalues is lost because the

2.3. Nematode community analyses correspondence between the eigenvalue and the structure along

each individual axis is lost. Therefore, an after-the-fact coefﬁcient

Upon arrival in the laboratory, a portion of the soil sample of determination between relative Euclidean distance in the unre-

to be used for nematode extraction was rehydrated and stored duced species space and Euclidiean distance in the ordination space

◦

at room temperature (23 C) for 48 h to hatch nematode eggs was performed for each axis yielded by each individual DCA to eval-

and activate dormant, anhydrobiotic nematodes. The moistened uate the effectiveness of each ordination in explaining variation

◦

soil was then stored for 3–4 days at 15 C prior to extraction. within the data (McCune and Mefford, 2006).

Nematodes were extracted by elutriation-centrifugal ﬂotation The nematode fungivore/bacteriovore ratio (FB ratio) was used

(Jenkins, 1964; Byrd et al., 1976) and quantiﬁed per 100-cm to gain insight into nutrient cycling via detrital pathways and the

volume of soil. An aliquot of each extracted sample was placed successional stage of the decomposer community. For the purpose

on a chambered counting slide and examined on an inverted of this analysis, we have categorized nematodes in the subfam-

Olympus IX51 compound microscope. Trophic groupings were ily Tylenchinae as a fungivore based on previous studies that have

categorized as bacteriovores, omnivores, fungivore, herbivores, identiﬁed the genera to feed upon the fungal energy pathway (e.g.,

carnivores, and Tylenchinae. Herbivore species were categorized Okada et al., 2002; Okada and Kadota, 2003; Okada et al., 2005).

into Tylenchinae (ectoparasite), Tylecnchorhynchus (ectopara- The bacteriovore/bacteriovore + herbivore ratio (BH ratio) was cal-

site), Paratylenchus (ectoparasite), Helicotylenchus (ectoparasite), culated in order to gather information about the grazing nematode

Criconemella (ectoparasite), Trichodorus (ectoparasite), Hoplolaimus and plant parasitic communities. Herbivorous nematode vs. the

(ectoparasite), Pratylenchus (migratory endoparasite), and Meloido- total nematode population (HT ratio) was also calculated in order

dera (sedentary endoparasite). In the 2010 samples, Tylenchinae to assess the total proportion of the herbivore community among

was grouped into two distinct groups based on morphological char- the three vegetation states that make up the desertiﬁcation gra-

acteristics and are indicated as Tylenchinae 1 and Tylenchinae 2. dient. All three ratios were calculated for both 2009 and 2010 JER

Tylenchinae was categorized independently from other trophic samples. The calculated ratios were then subjected to univariate

groupings because of the niche breadth of this subfamily and (ANOVA) analyses using LSD post hoc tests to look for differences

the multiple energy channels that constituent genera have been among vegetation states. The FB ratio was log transformed to meet

observed to feed upon. Debate has arisen in the scientiﬁc literature the assumptions of ANOVA.

as to what trophic category is appropriate to use when categorizing Shannon’s index of diversity (H) was used to assess the nema-

members of the subfamily Tylenchinae because different species tode diversity at each location across the established desertiﬁcation

have been observed to feed on algae, mosses, lichens (both fungal gradient and Otero Mesa soils for both trophic groups and herbi-

and ﬁlamentous cyannobacterial components), and are often times vore genera. Index values were then averaged by vegetation state.

the most abundant mycophagous species in the soil (Okada et al., Species evenness (E) was calculated using the same desertiﬁcation

2002; Okada and Kadota, 2003; Okada et al., 2005). gradient on the JER and Otero Mesa soils in order to look at the equi-

Herbivorous nematodes were further identiﬁed to genus for tability of nematode communities associated with each vegetation

both sampling years. A detrended correspondence analysis (DCA) state.

was used to compare nematode counts from soils across the Multivariate (MANOVA) analyses using Wilks’ Lambda multi-

desertiﬁcation gradient established at the JER for both trophic variate test statistic were conducted within sampled vegetation

and herbivore groupings during both sampling years, a compos- states to compare bare areas with vegetated areas. For this analysis,

ite JER analysis, and in a combined analysis with samples from both trophic groupings and herbivore genera from both sampling

the Otero Mesa grassland soils. The DCA used downweighted rare years were grouped and analyzed separately Grassland samples

70 J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77

collected from Otero Mesa were included with the data from the information can be gathered on herbivore community assem-

JER for this analysis. Post hoc tests were conducted to look at indi- blages based on the amount variation explained by the ﬁrst and

vidual species and trophic grouping differences within sample sites additional axes from the DCA analysis (Axis 1, r = 0.014; Axis

2 2

using least signiﬁcant differences (LSD). 2, r = −0.014; Axis 3, r = 0.000). High herbivore diversity was

observed in both the ecotone (H = 0.972) and the black grama grass-

land (H = 0.908) and substantially decreased within the mesquite

3. Results duneland sites (H = 0.219) and was signiﬁcantly different among

vegetation states (F = 19.791, p < 0.001, r = 0.457). Herbivore even-

3.1. Desertiﬁcation analysis ness was signiﬁcantly different among vegetation states (F = 6.229,

p = 0.004, r = 0.229) and highest in the ecotone (E = 0.845) followed

Each vegetation state along the desertiﬁcation gradient har- by the black grama grasslands (E = 0.701) and substantially lower

bored distinct nematode communities (Fig. 2a and b). The MRPP in the dune vegetation states (E = 0.288).

conducted on the DCA trophic scores validated these differences When Otero Mesa black grama grassland samples were included

(overall: A = 0.237, p < 0.001; pairwise comparisons: dune vs. eco- in the 2010 trophic and herbivore DCA, groupings aligned with the

tone: A = 0.129, p = 0.004; dune vs. grassland: A = 0.279, p < 0.001; black grama nematode communities taken from the JER within

ecotone vs. grassland: A = 0.108, p = 0.004). The effectiveness of ordination space (Fig. 3a and b), however, differences emerge

the ordination decreased as each higher axis was added (Axis 1, when the MRPP data is considered. Trophic analysis shows the

2 2 2

−

r = 0.230; Axis 2, r = 0.046; Axis 3, r = −0.015). Trophic diver- Otero Mesa (OM) nematode community structure to be signiﬁ-

sity was found to be signiﬁcantly different among vegetation cantly different when compared with the desertiﬁcation gradient

states (F = 5.289, p = 0.011, r = 0.261) and highest in the ecotone sampled on the JER, including the black grama grassland (overall:

vegetation state (H = 1.106) followed by the mesquite vegeta- A = 0.232, p < 0.001; pairwise comparisons: dune vs. OM: A = 0.352,

tion state (H = 0.772) and the black grama grassland (H = 0.680). p < 0.001, grassland vs. OM: A = 0.035, p = 0.029, ecotone vs. OM:

Trophic evenness was not found to be signiﬁcant among veg- A = 0.178, p < 0.001). Except for the ﬁrst axis, no cumulative varia-

2 2

etation states (F = 1.703, p = 0.199, r = 0.102) but was shown tion was explained by the successively higher axes (Axis 1, r = 0.12,

2 2

to be highest in the ecotone (E = 0.769) followed by the black Axis 2, r = −0.26, Axis 3, r = −0.24). Nematode trophic diversity

grama grassland (E = 0.644) and the mesquite duneland (E = 0.596). was signiﬁcantly different among all vegetation states (F = 25.433,

The herbivore analysis on the 2009 JER samples also showed p < 0.001, r = 0.556) the highest recorded value among all sample

very distinct groupings of species with vegetation (Fig. 2b). The locations (H = 0.978) and species evenness was slightly lower that

MRPP conﬁrmed that there were signiﬁcant differences in the the ecotone vegetation state sampled on the Jornada (E = 0.714)

nematode community associated with each vegetation state (over- but found not to be signiﬁcant among sample locations (F = 0.194,

all: A = 0.430, p < 0.001; pairwise comparisons: dune vs. ecotone p = 0.900, r = 0.010). Herbivore communities were found to be very

A = 0.174, p < 0.001; dune vs. grassland: A = 0.473, p < 0.001; eco- similar among Otero Mesa and JER black grama grassland sam-

tone vs. grassland: A = 0.430, p < 0.001). Axis 1 (r = 0.169) and Axis 2 ples (Fig. 3b) and the pairwise comparison of MRPP scores indicate

(r = 0.063) cumulatively accounted for 23.1% of the variance asso- that these two communities are not signiﬁcantly different (overall:

ciated with the herbivore species data, where the addition of a A = 0.125, p = <0.001; pairwise comparisons: dune vs. OM: A = 0.179,

third axis (r = −0.014) provided no additional information. Herbi- p < 0.001; grassland vs. OM: A = 0.004, p = 0.301; ecotone vs. OM:

vore diversity was signiﬁcantly different among vegetation states A = 0.052, p = 0.017). Again, two distinct Tylenchinae genera were

(F = 7.836, p = 0.002, r = 0.359) with the highest in the ecotone observed and enumerated separately. Variation increased with the

vegetation state (H = 1.24) followed by the black grama grass- inclusion of the Otero Mesa samples, where the ﬁrst and higher axes

2 2

land (H = 0.639) and the mesquite duneland (H = 0.542). Herbivore accounted for minimal variance (Axis 1, r = 0.07, Axis 2, r = 0.06,

species evenness was found to be signiﬁcantly different among Axis 3, r = −0.04). The Otero Mesa soils had the highest measure

vegetation states (F = 4.235, p = 0.025, r = 0.232) and highest in of herbivore species diversity of all samples analyzed (H = 1.242)

the ecotone (E = 0.850) and lowest in the black grama grassland and species evenness was relatively high as well (E = 0.776). When

(E = 0.558) with evenness in the mesquite duneland intermediate Otero Mesa samples were compared with the Jornada herbivore

between the other two vegetation states (E = 0.0603). species diversity and evenness analysis, all vegetation states were

The desertiﬁcation gradient sampled on the JER in 2010 showed found to signiﬁcantly differ (H: F = 25433, p < 0.001, r = 0.556; E:

results similar to the 2009 sampling in that nematode communities F = 5.966, p = 0.001, r = 0.242).

were found to be signiﬁcantly different among the three vegetation When the two sampling years of the desertiﬁcation gradient

states except with the ecotone and mesquite duneland compar- on the JER were combined to form a composite data set, the same

ison were not signiﬁcantly different, as indicated by the MRPP general patterns were observed as in the individual sampling year

(overall: A = 0.158, p < 0.001; pairwise comparisons: dune vs. eco- analyses—e.g., signiﬁcant differences in both trophic and herbi-

tone: A = 0.030, p = 0.064; dune vs. grassland: A = 0.230, p < 0.001; vore groupings among vegetation states (Fig. 4a and b; Trophic

grassland vs. ecotone: 0.088, p = 0.006). Trophic diversity was sig- MRPP Analysis: overall: A = 0.190, p < 0.001; pairwise comparisons:

niﬁcantly different among vegetation states (F = 6.066, p = 0.005, dune vs. ecotone, A = 0.066, p = 0.001; dune vs. grassland, A = 0.254,

r = 0.205) and highest in the ecotone (H = 0.952) as was even- p < 0.001; ecotone vs. grassland: A = 0.095, p < 0.001; Herbivore

ness (E = 0.740). B. eriopoda grassland trophic diversity was found MRPP Analysis: overall: A = 0.127, p < 0.001; pairwise comparisons:

to be intermediate in both diversity and evenness (H = 0.742; dune vs. ecotone: A = 0.084, p < 0.001, dune vs. grassland: A = 0.129,

E = 0.684) between the ecotone and mesquite duneland (H = 0.580; p < 0.001; ecotone vs. grassland: A = 0.075, p < 0.001). The variation

E = 0.647) where there evenness was not signiﬁcant among all three explained was only relegated to Axis 1 and Axis 2 (Axis 1, r = 0.06,

2 2 2

vegetation states (F = 0,228, p = 0.797, r = 0.010). Herbivore sam- Axis 2, r = 0.044, Axis 3, r = −0.03). There was some inter-annual

pling also showed distinct nematode communities associated with variability in nematode communities from one year to the next,

vegetation state (Fig. 4b; overall: A = 0.158, p < 0.001; pairwise com- with the 2009 sampling year yielding signiﬁcantly more nematodes

parisons: dune vs. ecotone A = 0.090, p = 0.001; dune vs. grassland: in both trophic (Wilk’s Lambda, F = 3.937, Value = 0.514, p = 0.007)

A = 0.214, p < 0.001; ecotone vs. grassland: A = 0.053, p = 0.012). The and herbivore (Wilk’s Lambda, F = 2.903, Value = 0.699, p = 0.040)

2010 samples yielded two predominant genera within the sub- analyses for the dune vegetation state as well as the herbivore

family Tylenchinae that were classiﬁed separately. However, little analysis for the ecotone (Wilk’s Lambda, F = 2.714, Value = 0.409,

J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77 71

Fig. 2. DCA of nematode trophic (a) and herbivore sampling (b) of the JER desertiﬁcation gradient in 2009. Nematode species DCA scores are represented as vectors on the

bottom panels for both trophic and herbivore groupings.

p = 0.046) vegetation state where there were signiﬁcantly more E = 0.679) and lastly the mesquite duneland site (Trophic, H = 0.651,

Criconemoides spp. (Value = 7.508; p = 0.012) and Hoplolaimus spp. E = 0.628; Herbivore, H = 0.340, E = 0.406). Trophic diversity was

(Value = 13.569; p = 0.001) were recovered in 2009 than 2010. found to be signiﬁcantly different among vegetation states when

However, there were no signiﬁcant differences observed in the the composite Jornada samples were compared (F = 9.236, p < 0.001,

2 2

nematode communities associated with the black grama grass- r = 0.190) but evenness was not (F = 1.238, p = 0.295, r = 0.030).

lands from one year to the next. The dune trophic analysis showed Overall, all three calculated ratios differed signiﬁcantly among

that signiﬁcantly greater numbers of bacteriovores (F = 15.451, the three vegetation states on the JER (Table 2). Post hoc

2 2

p < 0.001, r = 0.340), tylenchus (F = 9.793, p = 0.004, r = 0.246), and tests revealed that the FB ratio was signiﬁcantly different

herbivores (F = 18.040, p < 0.001, r = 0.376) in 2009 than 2010 sam- between the black grama grassland and the mesquite duneland

ples and in the herbivore analysis there were signiﬁcantly more (LSD, p = 0.006) with more fungivores present in the grassland

Meloidodera spp. (F = 11.317, p < 0.001, r = 0.303) in 2009 than in 2010.

Table 2

In the 2010 herbivore sampling, two distinctly different genera Univariate analysis of calculated nematode ratios from the Jornada for both 2009 and

of Tylenchinae were observed based on morphological characteris- 2010 sampling years combined as well as the Otero Mesa sampling from 2010: fungi-

vore:bacteriovore ratio (FB), herbivore:bacteriovore ratio (HB), and herbivore:total

tics, but have yet to be deﬁnitively classiﬁed. However, for purposes

nematode population ratio (HT). All calculated ratios signiﬁcantly differed among all

of this analysis these two genera were combined into the com-

vegetation states along the desertiﬁcation gradient and the undisturbed grassland

mon subfamily Tylenchinae due to similarity in trophic behavior. samples.

Trophic and herbivore species diversity and evenness was also con-

Ratio F p R

sistent with results from the 2009 analyses in that the ecotone

was found to be the most diverse (Trophic, H = 1.010; Herbivore, FB 12.886 <0.001 .213

HB 39.356 <0.001 .453

H = 1.028) as well as having the most evenly distributed species val- **

HT 38.134 <0.001 .445

ues (Trophic, E = 0.751; Herbivore, E = 1.144) followed by the black

Indicates signiﬁcance at the ˛ = 0.001 level.

grama grassland (Trophic, H = 0.715, E = 0.749; Herbivore, H = 0.751,

72 J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77

Fig. 3. DCA of nematode trophic (a) and herbivore sampling (b) of the JER desertiﬁcation gradient in 2010 as well as grassland samples from Otero Mesa sampling in 2010

as well. Nematode species DCA scores are represented as vectors on the bottom panels for both trophic and herbivore groupings.

vegetation state (dune = 0.096; ecotone = 0.273; grassland = 0.373). ecotone vegetation state (Table 3). The between subject effects of

The BH ratio differed among all vegetation states where signiﬁ- the herbivore analysis did reveal a differences in the distribution of

cantly more bacteriovores were found in the dune (0.225) > ecotone Hoplolaimus species (F4,22 = 3.144, p = 0.040, r = 0.411) where post

(0.533) > grassland (0.714) (LSD, dune vs. grassland: p < 0.001, dune hoc tests showed signiﬁcantly more species associated with sam-

vs. ecotone: p = 0.029, grassland vs. ecotone, p = 0.001). The HT ples taken from soils with co-occurring mesquite and black grama

ratio also showed signiﬁcant differences in herbivorous nema- (LSD, p = 0.048). No signiﬁcant differences were detected in the eco-

todes across all vegetation states with the most herbivores in tone trophic analysis among sampling locations (Table 3). However,

the grassland (0.232) > ecotone (0.369) > dune (0.649) (LSD, dune vs. bacteriovores were found to be signiﬁcantly more prevalent within

grassland: p < 0.001, dune vs. ecotone: p = 0.023, grassland vs. eco- soils associated with P. glandulosa than B. eriopoda or where these

tone: p < 0.001). Because the data was log transformed to meet the species co-occurred (F4,23 = 5.904, p = 0.003, r = 0.550).

assumptions of ANOVA, post hoc tests were not performed because Only bacteriovore trophic groupings in dune vegetation were

at least one group had fewer than two cases. signiﬁcantly different from interdune areas (F3,32 = 2.970, p = 0.049,

r = 0.241), and no overall effect of sample location was observed

3.2. Plant-interspace analysis (Table 3). However, when sampling location on the dune is not

accounted for and trophic groupings are compared between dune

The MANOVA analysis was conducted on both trophic and her- and interdune bare ground gap samples, numbers of bacteriovores

bivore nematode groupings analyzed across microsite locations and Tylenchinae genera differed signiﬁcantly with fewer num-

among the vegetation states along the desertiﬁcation gradient. bers in the interdune areas (Bacteriovores, F1,32 = 9.458, p = 0.004,

2 2

The grassland samples showed no signiﬁcant differences in nema- r = 0.24; Tylenchinae, F1,32 = 7.081, p = 0.012, r = 0.191). No omni-

tode trophic and herbivore groupings among black grama patches, vores, fungivore, or carnivores were found in the interdune areas

soil gaps with soil biotic crusts, and bare ground across loca- and herbivores were lower when compared with the mesquite

tions (Table 3). Multivariate tests showed no differences in trophic dune nematode community. Herbivore communities were signif-

and herbivore groupings among sampling locations within the icantly different among samples taken from the mesquite dune

J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77 73

Fig. 4. DCA of nematode trophic (a) and herbivore sampling (b) of the JER desertiﬁcation gradient in 2010 and grassland samples from the Otero Mesa sampling in 2010.

Nematode species DCA scores are represented as vectors on the bottom panels for both trophic and herbivore groupings.

and the interdune areas as well (Table 3). Only four species of Paratylenchus spp. was found in the interdune areas, and low recov-

the nine genera of herbivores identified throughout the desertifi- ery of this genus within the dune itself failed to support significant

cation gradient (Meloidodera, Tylenchorhynchus, Paratylenchus, and differences among locations.

Tylenchinae) resided within the dune vegetation state. All nema-

tode herbivores associated with the dune vegetation state occurred 4. Discussion

in much lower numbers, if at all, within interdune areas. Num-

bers of Tylenchorhynchus spp. were signiﬁcantly lower in interdune The extensive biodiversity retained within soils is fundamen-

areas (LSD, p = 0.034) as were Tylenchinae spp. (LSD, p = 0.020). No tal to maintain plant productivity, yet soils as a living natural

Table 3

MANOVA analysis of the effects of sampling location for each of the three vegetation states on nematode groupings along the desertiﬁcation gradient on the JER using Wilk’s

Lambda. Numbers within parentheses in the dune vegetation are indicative of nematode communities where the multivariate analysis did not account for dune architecture

and only relegated samples to either dune or interdune samples.

Vegetation Analysis F Value df p

Trophic 0.810 0.716 15 0.664

Grassland

Herbivore 0.720 0.718 64 0.764

Trophic 1.348 0.176 24 0.184

Ecotone

Herbivore 1.435 0.066 32 0.135

Trophic 1.162 (2.008) 0.457 (0.675) 18 (6) 0.318 (0.103)

Dune *

Herbivore 2.123 (0.904) 0.340 (0.717) 15 (10) 0.019 (0.537)

Indicates signiﬁcance at the ˛ = 0.05 level.

74 J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77

resource are often ignored in issues of state changes where only black grama grasslands, aiding in drought tolerance, and enhancing

rudimentary knowledge of soil biotic diversity is known for a few nutrient uptake from shallow calcareous soils. Coupled with these

ecosystem types (Brussaard et al., 1997; Wall and Virginia, 1999; effects, plant parasitic nematodes are involved in the transfer of

Bardgett et al., 2005; Sylvain and Wall, 2011). Our analysis of photosynthetically ﬁxed carbon and organic compounds into the

nematode community structure supports the hypotheses that the rhizosphere that affect nutrient dynamics and microbial biomass

desertiﬁcation of B. eriopoda grasslands through the encroachment that ultimately have the potential to have ecosystem level effects

by mesquite shrubs has altered nematode communities, and (Ingham and Coleman, 1983; Ingham et al., 1985; Bardgett et al.,

caused them to become more heterogeneous and less diverse. 1998; Yeates, 1999). The sheer number of plant parasitic nema-

Increases in bare ground gaps that accompany desertiﬁcation have todes found to reside within the black grama grasslands sampled

relegated the majority of nematodes to communities associated in this study does not appear to be severely impacting the produc-

with vegetated patches. Furthermore, the incidence of speciﬁc tion of these grasslands, especially those occurring on Otero Mesa.

nematode genera aligning with vegetation states along our deser- However, the coupled affect of large herbivorous nematode pop-

tiﬁcation gradient support the “fungal loop” model proposed to ulations, drought, intermittent disturbances, and low fecundity of

translocate C, N, P, and mineral nutrients among resources patches black grama (Peters, 2002b) could combine to have a detrimental

and sustain ecosystem productivity in similar grassland systems effect on black grama and may be attributing to the desertiﬁcation

(Collins et al., 2008; Green et al., 2008). of this arid grassland. Further information is needed to quantify the

larger impacts of plant parasitic nematodes on plant production in

4.1. Desertiﬁcation effect this system and natural systems as a whole.

The high nematode diversity observed in the ecotone can be 4.2. Plant-interspace effects

explained by ecological niche partitioning. Increases in resources

due to multiple plant life forms (grasses and shrubs) may have With the lowest observed diversity and reduced numbers of her-

provided more microhabitats and energy channels for increased bivores genera, signiﬁcant decline in bacteriovores, as well as the

nematode diversity and subsequently, soil biota that has increased absence of Tylenchinae, omnivores, fungivores, and carnivores with

functional redundancy caused by decreases in competitive exclu- the interdune areas compared with mesquite dunes themselves

sion (Armstrong and McGehee, 1980; Freckman and Virginia, 1989). illustrates the inﬂuence of vegetation on nematode community

Less diverse, more specialized nematode communities diverge structure. The loss in connected vegetation and increases in inter-

from ecotone community assemblages and align with the vegeta- space gaps characteristic of the desertiﬁcation of arid grasslands

tion speciﬁc to either B. eriopoda or P. glandulosa and occupy speciﬁc has caused nematode abundance to become patchier. This frag-

functional roles resulting in increased competition. mentation has undoubtedly affected prey guilds as indicated by

Our results show that once P. glandulosa has encroached on, and nematode community assemblages and their spatial distributions

replaced areas previously dominated by grasses, the species guild of within the shrub dominated vegetation state (Fierer and Jackson,

herbivorous nematodes is dominated by very speciﬁc species with 2006; Housman et al., 2007). Due to limitations in their coloniza-

relatively few remaining representatives of the B. eriopoda grass- tion abilities, nematode community assemblages are indicative

land. Furthermore, trophic complexity becomes largely relegated of shifts in species dominance and because of their central role

to ﬁrst order grazers (bacteriovores) in the dunelands and becomes in food-web dynamics, these changes in nematode community

highly dependent on the spatial distribution of fragmented vege- assemblages serve as a corollary for changes in the soil biotic con-

tation patches. These shifts in dominance to a few genera signify sortia once shrubs become dominant further altering ecosystem

alterations in plant–soil biotic associations within the differing veg- processes (Kardol et al., 2005).

etation states. However, it is not clear how this change in the soil The high proportion of bacterial feeding nematodes found

biotic community becomes initiated or what the direct effects to within the mesquite vegetation state has the potential to severely

the plant community. alter the nutrient dynamics, especially nitrogen, both directly

Further support for nematode communities aligning with and indirectly and may be accentuating the “islands of fertility”

vegetation distributions is apparent in the lack of signiﬁcant observed by Schlesinger et al. (1990). Studies have shown that dis-

differences between herbivore communities from the JER black turbance has lead to shifts in the microbivorous nematodes from

grama sites and the Otero Mesa black grama grassland sam- predominantly fungivores to predominantly bacteriovores mirror-

ples. High diversity observed within the Otero Mesa site may be ing energy channel shifts (Hendrix et al., 1986; Moore and de Ruiter,

related to the lack of impact from long-term grazing combined 1991; Darby et al., 2010). These shifts are important because nema-

with a more stable geomorphic surface. Because these two sites todes directly secrete ammonium as a byproduct of metabolism

are geographically separated by approximately 160 km, yet har- of prey guilds that possess lower C:N ratios than required by

bor similar herbivore/plant-parasitic communities, illustrates the nematodes themselves (Neher, 2010). This excess nitrogen is read-

broad landscape-scale distribution patterns of nematode com- ily available for plant uptake but also can stimulate increased

munities in the Southwest and are perhaps indicative of the growth of microbial populations and lead to enhanced microbial

importance of soil biofeedbacks in semi-arid grasslands. turnover and dispersal where moderate grazing by nematodes can

Native plants are more resistant and tolerant to nematode par- even further stimulate microbial growth (Yeates, 1999; Neher,

asitism when compared to plants grown in agricultural settings 2010). Increased N mineralization rates in the bacterial decom-

based on evolutionary histories and co-evolution, competition, position channel compared to the fungal decomposition channel

arbuscular mycorrhizae and endophytic fungi that act as biocon- lead to greater losses of nitrogen through volatilization. Therefore,

trol agents (Wallace, 1987; Neher, 2010). Furthermore, lateral root systems with high bacterial populations may be prone to large

production has been shown by plants responding to herbivory nitrogen deﬁcits when compared with other soil microbial systems

by nematode populations along with increased root exudation (Peterjohn and Schlesinger, 1991; Darby et al., 2010; Neher, 2010).

that can affect plant nutrient uptake as well as nutrient cycling The fungivore to bacteriovore ratio (FB ratio) has been widely

(Freckman and Virginia, 1989; Moore et al., 2003). Also, wound- accepted to yield insight into the successional stage of the decom-

ing of roots by nematodes may provide increased infection sites poser community. However, the incidence of the translocation of

for symbiotic fungal infections to occur (Freckman and Virginia, C from plant patches to adjacent crust patches via DSF and sapro-

1989), thus perpetuating the connectivity among plant patches in torphic fungi and with the biotic ﬁxation, increased mineralization

J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77 75

and mobilization of N by the cyannobacterial component of crusts, Tylenchinae community. Also, DSF endophyte extensions from

the FB ratio is indicative of other process outside of decomposition black grama patches involved in the translocation of C and N

(Evans and Ehleringer, 1993; Hawkes, 2003; Green et al., 2008). As are linked to soil biotic crusts in plant-interspaces reinforcing the

the interactions of fungi and environmental conditions above and even distribution of Tylenchinae among vegetated and bare-ground

below ground limit organic nutrient accumulation, the net effects patches (Green et al., 2008). We acknowledge that Tylenchinae are

of a highly connected ecosystem exist in a tightly integrated sys- not feeding on the traditional AMF and ectomycorrhizal energy

tem of primary producers and heterotrophs (Collins et al., 2008; channels as many indices suggest, but feed on the endophytic dark

Crenshaw et al., 2008). While nutrient levels in black grama grass- septate fungi and soil biotic crust components of these semi arid

lands are much lower when compared with duneland vegetation grasslands (Kohn and Stasovski, 1990; Barrow, 1997; Barrow et al.,

patches, the increased connectivity among vegetation patches and 2004; Porra-Alfaro et al., 2008; Herrera et al., 2010). These fac-

biotic crusts in arid grasslands has the potential to retain nutrients tors led us to calculate the FB ratio in this study after classifying

and positively feedback amongst the biotic pathways classiﬁed by members of the Tylenchinae as fungivores.

the fungal loop model and distribution of soil biota.

5. Summary and conclusion

4.3. Interpretation of Tylenchinae

While many unknowns exist in the evaluation of nematode

In this study, members of the subfamily Tylenchinae accounted

populations within natural systems, previous research along with

for 16% and 17% of the soil nematode communities in 2009 and

results from this study provide information in the role of soil biota

2010, respectively. Other studies have shown that the Tylenchi-

in desertiﬁcation of arid grasslands. The shift in soil community

nae account for up to 30% of such communities (Okada and Kadota,

structure and the subsequent change in soil biotic energy path-

2003). Differing trophic classiﬁcations have important implications

ways, associated with desertiﬁcation can lead to ecosystem level

when summarizing the ecological roles of Tylenchinae or when

alterations of nutrient cycling and changes in aboveground pro-

using indices based on arbitrarily assigned trophic classiﬁcations

duction (Bardgett et al., 1998). As desertiﬁcation increases, soil

to assess soil quality, ecosystem function, nutrient cycling, and the

biotic populations become less diverse and more heterogeneously

impact of disturbance (Wright and Coleman, 2000). Tylenchinae are

distributed in vegetation patches that further alter nutrient dynam-

not generally considered to be signiﬁcant root parasites and their

ics on an ecosystem scale (Schlesinger et al., 1990). Furthermore,

relative prominence in this study may provide more information as

loss of the associated soil biotic consortia that is intimately tied

an indicator of speciﬁc ecosystem processes such as the fungal loop

to ecosystem function of semi-arid grasslands may have real and

hypothesis (Siddiqi, 2000; Collins et al., 2008). As nematodes play a

long-term consequences for the sustainability and recovery of B.

central role in soil food web dynamics, nematode assemblages are

eriopoda grasslands.

distributed in patches centered on available resources.

A more diverse trophic structure, as observed in the Otero

It appears that desertiﬁcation may disrupt vital plant–soil inter-

Mesa soils, may be indicative of stability in ecosystem interac-

actions that are characteristic of B. eriopoda grasslands where

tions between roots and the fungal and bacterial energy channels

Tylenchinae feed mainly upon fungi, algae, and lichens and where

(Moore et al., 2003). Dominance of any one energy channel might

there are no differences in the distribution of this subfamily

be indicative of dynamic instability as observed within the JER

between vegetated patches and plant-interspaces in these grass-

grassland (fungal) and the mesquite duneland (bacterial), where

lands (Siddiqi, 2000; Okada et al., 2005). However, in vegetated

unimpeded vertical energy ﬂow may provide increased nutrient

mesquite dunes Tylenchinae numbers were signiﬁcantly lower

supplies, nutrient imbalance or losses, and a change in facilitative

than in black grama grasslands and virtually absent from inter-

soil biotic communities vital to plant production and resilience in

dunal areas in the mesquite dominated vegetation state that is

arid systems (Moore et al., 2003; Darby et al., 2007, 2010). How-

essentially void of soil biotic crusts and provides further evidence

ever, the dominance of the fungal energy channel in black grama

of the disruption of vital soil biofeedbacks by desertiﬁcation and

grasslands on the Jornada may be indicative of a fully functioning,

shrub establishment. If Tylenchinae were feeding primarily on

connected system of hyphal networks, plant patches and soil biotic

higher plants in these arid systems, we would expect the com-

crusts.

munities to be similar among vegetation states or at least among

Linking nematode populations and trophic structure to function

vegetated patches. Furthermore, mesquite dunes contain an assort-

at individual plant scales is more complex than just enumera-

ment of associated plants such as saltbush (Atriplex canescens),

tion and identiﬁcation because of their central role in food webs

broom snakeweed (Gutiereza sarothrae), dropseeds (Sporobolus

and connections to ecological processes in soil (Neher, 2010). In

spp.), threeawns (Aristida spp.), and a variety of forbs that serve

order for nematode community and trophic analyses to be more

as food sources for herbivorous nematodes (Peters and Gibbens,

useful, a more complete understanding of feeding habits and tol-

2006). The greater abundance of Tylenchinae where soil biotic

erance levels of each dominant nematode genus to abiotic stresses

crusts are present reinforces grouping Tylenchinae separately from

are needed before soil nematode community indices can be inter-

other conventional herbivore genera and supports their utilization

preted and calibrated accurately as indicators of arid land soil

of photosynthetically active algal and cyannobacterial lichenous

condition, function, and soil biotic interactions (Darby et al., 2007).

components as well as the fungal symbiont that comprise these

This improved understanding will require improved species level

crusts as substrate opposed to feeding largely as true parasites of

identiﬁcation using morphological and molecular criteria, where

higher plants.

life history information relating to speciﬁc environments can be

While some members of the Tylenchinae may occasionally feed

applied to community level surveys.

as herbivores, as their low numbers within the mesquite dunes that

are void of soil biotic crusts may indicate, we believe that the abun-

dance of the Tylenchinae community in sites lacking vascular plants Acknowledgements

is indicative that they are typically not feeding as conventional

herbivores in this study. The consolidated matrices of soil biotic We would like to thank the Nematology Lab at New Mexico

crusts characteristic of areas vegetated with black grama and the State University for their assistance in data collection and sam-

plant-interspaces between create a more homogenous, connected ple processing, Dr. Ernest Bernard, and Zachary Sylvain for critical

cover in the grasslands allowing for a more evenly distributed review of our manuscript. Funding support was provided by the

76 J.R. Klass et al. / Applied Soil Ecology 58 (2012) 66–77

National Science Foundation to New Mexico State University as part Herrera, J., Khidir, H.H., Eudy, D.M., Porras-Alfaro, A., Natvig, D.O., Sinsabaugh, R.L.,

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