Opinions and Suggestions on Nematode Faunal Analysis

In formulating the MI, Bongers (1990) omitted plant-feeding taxa but calculated a separate Plant-Parasitic Index (PPI). He noted that when plants are good hosts for c-p3 plant parasites, the relationship between MI and PPI may be inverse (Bongers et al., 1997; Du Preez et al., 2022). On the other hand, in ecosystems with high plant diversity, the inverse relationship between MI and PPI may not occur (Neher and Campbell, 1996). Yeates (1994) and others argued for an alternative, ΣMI, in which plant-parasitic species are included.

The abundance and nature of plant-feeding nematodes impact the productivity of soil ecosystems and provide resources for predator organisms. The contribution to soil nutrient availability of root-hair feeders and other less-damaging parasites may offset any damage caused to plant growth. We believe an important enhancement of the faunal analysis model is the inclusion of a Herbivory Index (HI) based on the feeding habits and damage potential of plant-parasitic species. Interpretation of the herbivory component would be aided by developing a framework consistent with other dimensions of the faunal analysis model.

Yeates et al. (1993) recognized six h-c categories of plant-feeding nematodes based on their feeding habits. We use the h-c designation for terminological consistency with the c-p designations. We propose using the h-c categories to develop a weighting system based on the probable carbon turnover rates (Table 1A). The body weights of adult females are determined from morphometric data and are available as feeding category averages in Nemaplex (Nemaplex. ucdavis.edu). Refinements of the weighting system will occur as new information on feeding habits and damage potential of taxa emerges. We calculate the herbivory channel by weighing the abundance of nematodes in each category as a percentage of the carbon being processed if all nematodes present were in h-c6, the sedentary endoparasites. So, HI =100 (Σ hc_i n_i) / (hc₆ Σ n_i), where i represents the 1 to 6 h-c weight classes of plant-feeding nematodes present in the assemblage (Table 1B). That allows a maximum value for carbon processed through the herbivory channel of 100. The Herbivory Index is integrated into the Emended Faunal Analysis Model using the Structure Index as the abscissa (Figs. 1 B,C). Some interpretive criteria are provided in Box 2; see also, Ferris et al., 2001.

Determination of the HI will require a few extra steps in the nematode abundance assessment. The abundance of ectoparasitic plant feeders can be determined through the extraction process used for free-living taxa. The abundance of sedentary and semi-endoparasitic nematodes can be determined as the number of egg masses, female bodies, or cysts on the root surface. If migratory endoparasites are present, mist chamber extraction of a root sample will also be necessary.

Reversion is a practice in which fields are retired from harvested production because their soils are considered damaged or depleted by conventional or high-input production practices. The area may be allowed to revert to the natural vegetation of that landscape with the hope that, in time, the physical, chemical, and structural nature of the soil will recover. Regeneration is a more managed conservation and rehabilitation process whereby resources are supplied that are considered necessary for the recovery of the soil. Practices include returning waste products of agricultural production to the soil and adding composted material from exogenous sources. Major goals include topsoil improvement, enhancing soil biodiversity, improving nutrient cycling, water porosity and drainage, biosequestration, and general enhancement of the productivity and viability of the soil. Degeneration, on the other hand, refers to changes in the soil that adversely affect those characteristics and generally reduce soil health by replacing its biological attributes with mineral fertilizers, pesticides, and tillage (Mitchell et al., 2024).

The productivity of anthropogenically modified or regenerative systems may require continued nurturing. Enhancements of the Structure and Enrichment Indices by organic amendment of field plots over a period of seven years were reversed in a single year during which organic amendments were terminated, and conventional agricultural practices were applied (Berkelmans et al., 2003). Unless the soil has an abundance of soil carbon, resources supplied by single applications of organic amendments are followed by a stimulus of the Enrichment Footprint and then a successional stimulus of the Structure Footprint, followed by a general decline in both as resources become depleted (Fig. 2B).

Herein, we use the term auto-regeneration to describe the hypothesized natural sequence of recovery in soil ecosystems, and their functional attributes, where residual soil carbon stocks remain and are amplified by new sources of rhizodeposition. We believe that auto-regenerative processes are accelerated in the humid tropics. In a study of the effects of clearing primary tropical forests and allowing regrowth of secondary forests or converting them to either tree plantations or pasture, analysis of nematode assemblages in the new systems was conducted in five locations in a national park system in Costa Rica (Varela-Benavides et al., 2022). Faunal analyses were based on 100 composite samples of 10 cores each, taken in the same year at each location. The expectation, based on the faunal analysis model, was for an enhancement of the Enrichment Index as soil was disturbed and decomposition resources were made available to soil organisms, and a diminution of the Structure Index depending upon the amount of disturbance involved in conversion to the new soil ecosystem (Fig. 3C). The analyses of nematode assemblages in the systems at the five locations involved the identification and enumeration of nematodes of some 135 taxa, 55 of which were considered abundant or very abundant. Rather than clearly reflecting the hypothesized degree of disturbance (Fig. 3A), the analyses revealed that the Structure and Enrichment Index were quite similar across locations and systems (Fig. 3B).

Figure 3:

A: Hypothetical effects of primary forest clearing; letters indicate expected locations of the intersection of enrichment and structure trajectories after the disturbances, W: residual primary forest, X: secondary forest, Y: tree plantation, Z: pasture; B: Actual Faunal Analysis of residual primary forest, secondary forest, tree plantation and pasture.; C: Hypothetical auto-regeneration of enrichment and structure indicator components of the soil food web after a major disturbance, note time scale differences; D: Consistency of c-p 4 and 5 taxa 3 to 30 years after a disturbance as a percentage of those in primary forest. Data from Varela-Benavides et al. (2022).

An important variable not considered in the Costa Rican study was the successional events between the original disturbance and the time of sampling of the systems. In this case, the intervals at the various locations between clearing the primary forest and sampling for nematodes in the new ecosystems ranged from 3 to 30 years. We believe that is enough time for auto-regenerative processes to stabilize to a steady state of ecosystem functioning, particularly in a humid tropical environment (Fig. 3C).

Conversion of primary forests to other production systems involves harvesting timber, clear-cutting vegetation, uprooting stumps, and burning residual debris. Following that, there may be some land-leveling with heavy equipment and either secondary forest regrowth or the establishment of commercial tree crops or grasses for pasture. While all those are significant disturbances, none would be enough to eliminate resident nematode species except, perhaps, for extremely host-specific plant parasites. Rather, organic matter decomposition pathways would become re-established. However, in different micro-patches of the soil environment, enrichment-opportunistic nematode taxa would flourish in a relatively short timeframe (Fig. 3C). Consequently, resources would become available for survivors of cohorts of disturbance-intolerant nematode omnivores and predators in the c-p4 and c-p5 structural guilds. Over varying periods, depending on the ecophysiological and behavioral characteristics of organisms in the various structural guilds, auto-regeneration of the soil food web would occur, probably initially with variable and chaotic fluctuations of organism abundance but eventually stabilizing to a functional equilibrium of resource availability and utilization (Fig. 3C). If, however, removal of the primary forest and its residues involved the use of toxic materials to certain components of the soil food web, regeneration of higher and sensitive trophic levels might not occur, or would occur very slowly (e.g., Korthals et al., 1996; 1998).

The subsurface residues of the cleared forest provide widely dispersed masses of carbon sources that gradually become separated into patches of diminishing sizes through decomposition processes at different rates. The multipartite succession of organisms would occur in each patch at different rates, which is determined partly by the status of the residual carbon-based source and rhizodeposition from new plant sources. When considering the whole system subjected to disturbance and regeneration, the individual populations in each patch constitute a series of metapopulations (Hanski and Ovaskainen, 2000). Measurement of the integral biological structure of the complex distribution of patches is, of course, a challenge. Soil sampling devices encounter diverse groups of patches, resulting in variable and unreliable assessments of species presence and abundance. However, from repeated composites of such samples, successional trends in the nematode metapopulations emerge (Fig. 3C).

Supporting the auto-regeneration hypothesis is that, based on the composite sampling procedures in the Costa Rican study, even with their inherent variability, between 35 and 60% of the disturbance-sensitive c-p4 and c-p5 taxa of the primary forest soil in each location were detected in the disturbed systems (Fig. 3D). Further, the metabolic footprints of predator and omnivore taxa of the c-p4-5 stress-intolerant groups were related to resource prey availability indicated by the Enrichment plus Herbivory Footprints (analysis not shown). In other words, the auto-regenerative process was autonomous in the ecosystems that became established during the 3 to 30 years that elapsed after removing the primary forest.

As a caveat to the auto-regeneration hypothesis, we believe that recovery of the systems would not occur or would occur very slowly if suppressed by anthropogenic influences or by natural or unnatural disasters that result in prolonged conditions toxic to higher c-p group nematodes. Suppression of auto-regeneration can be inferred from many studies. It occurs when soils contaminated by residues from industrial activities or by residues and spills from mining operations remain toxic to sensitive structure-indicator species (Korthals et al., 1996; 1998; Sánchez-Moreno et al., 2006; Shao et al., 2008). As a general observation, the abundance of c-p4-5 taxa is usually very low in soils subjected to long-term conventional agriculture. In those soils, unlike the experience in the conversion of primary forest in Costa Rica, the frequency of occurrence of structure-indicator taxa is much lower than encountered in surrounding undisturbed soils (Sánchez-Moreno and Ferris, 2007; Sánchez-Moreno et al., 2008; 2009). Efforts to re-introduce such taxa from undisturbed areas are unsuccessful, at least in the short term, possibly due to changes in soil structure, a significant reduction in root biomass and soil organic carbon, or effects of persistent accumulation of mineral fertilizers (Tenuta and Ferris, 2004; DuPont et al., 2009; Glover et al., 2010).