NTF elevational species richness and occurrence frequency pattern
In this study, we compared NTF species richness and occurrence frequency across an elevation gradient on two mountain ranges. Overall, we found species composition similar between the sites, with 11 of the 17 species collected in common. However, we found species abundance and elevational range differed between the sites; previous studies of NTF on Cangshan found community-level structural differences at different altitudes and aspects [20]. In our study, we found diversity of NTF on Cangshan and Gaoligongshan showed mid-elevation peak and decreasing patterns, consistent with many studies on species diversity across an elevation gradient.
While this finding contributes to the growing body of evidence for monotonic (decreasing) or unimodal (mid-elevation peak) diversity patterns found along elevational gradients, it does not provide an explanation for its occurrence. In general, it is quite possible any combination of universal interreacting factors, such as climate, space, evolutionary history or biotic process to be driving the observed patterns in NTF diversity across elevation. Patterns of elevational species richness often reflect the ecology of the taxonomic group [21, 22]. NTF at these sites are found in soil generally in low abundances and at low diversity in comparison to many other taxonomic groups. Considering the specialized feeding strategies and dependence on nematodes for food, NTF elevational diversity pattern may be driven by nematode abundance and diversity. Nematodes are the most abundant metozoans in the soil, highly diverse, and occupy numerous, often overlapping, ecological niches [23]. They are essential to soil processes (e.g., decomposition, nitrogen cycling), productivity, and may be used as bioindicators of soil condition [24]. Nematodes worldwide exhibit several elevation diversity patterns (e.g., irregular patterns, increases with elevation and mid-elevation peak [25–27]) and the nematode diversity or abundance at the two sites is largely unknown, so it is difficult to draw conclusions [. However, abundance and richness are commonly predicted to be highest in the most productive environments [28]. On both mountain ranges, temperature decreases with increasing altitude [29], along with soil depth and soil nutrients, which should decrease productivity, and consequently, species richness with altitude. Rainfall and soil water availability generally exhibit a mid-elevation maximum in this region. As productivity in the soil is closely related to these basic limiting factors of life, we might predict productivity, and consequently nematode abundance and richness, to be highest at some intermediate elevation, but likely in the lower half, which could be driving the diversity and abundance of NFT.
Yet, it is impossible for us to discount the potential effects of other area-related factors, such as the species-area relationship (monotonic decreasing) mid-domain effects (unimodal mid-elevation peak), community overlap (unimodal mid-elevation peak) and ecotone effects [2]. The species-area relationship (SAR) asserts that as survey area decreases, such as the upper limits of the mountain, number of species encountered will correspondingly reduce [2]; the mid-domain effect (MDE) states that if all species ranges are scattered randomly between the limits of the top and bottom of a mountain, there will be a greater number of overlapping species in the mid-elevations as a consequence of the geometric limitations of the top of the mountain and valley bottom [34]; the community overlap hypothesis assumes that the transitional zone where upper mountain communities overlap with lower mountain communities a mid-elevation diversity maximum occurs. The ecotone effect predicts diversity peaks at ecotones, with higher peaks at more significant ecotones. Currently, there is mixed support for these theories, and little support for these predictions as a single predictor [2]. Because NTF abundance is so low in the environment, the importance of area driven factors is difficult justify. From the available evidence, we suggest the predominate factors underlying NTF elevational richness pattern appear to be climatic and ecological interactions specific to the taxon; however, much more ecological research is necessary to better isolate the principal drivers.
Comparison of sampling modes
Some of the variation in elevational diversity patterns that has been reported in the literature is potentially an artifact of sampling patterns, scale of study and post-sampling treatment of data [4]; however, empirical examples demonstrating these problems are few. We found results of the elevational richness and frequency patterns of NTF depended on the sampling patterns (sampling modes), scale of study (total elevation range) and post-sampling treatment of data (removing anthropomorphically disturbed samples). These results support the argument of Lomolino and Mark(2010). In the distance sampling method, the OF of NTF conformed to mid-elevation peak pattern, and species richness met LPMP pattern; however, the elevation sampling methods obtained a totally different result that the OF and species number of NTF both showed a decreasing pattern. It suggests that sampling methods affect the observed pattern. Our results re-emphasize the importance of using robust sampling in developing species richness and OF models along environmental gradients.
Undoubtedly, in the process of studying the distribution patterns of species, increasing sampling efforts sees a consequent increase to a model’s accuracy [30]. However, when the sampling sites are unevenly distributed, the results will likely be biased. The equidistant sampling method along the sample line in Gaoligongshan resulted in sampling points that were not averagely distributed on the elevational gradient but concentrated in the middle altitude range, which probably caused the overestimation on the species richness of NTF in this area. The correlation analysis on the number of species and sample points indicated that they were strongly correlated with each other, thus this sampling pattern in which the sample points were concentrated in the middle altitude areas showed a mid-elevation peak pattern.
When using the evenly sampling method along the elevational gradient at Gaoligongshan, the elevational distribution of NTF showed a decreasing pattern, this method would not be affected by the distribution of sampling sites and the scale of studied region, thus the decreasing pattern was probably closer to the true situation of the elevational distribution of NTF. We used the same sampling method in Cangshan and got the same results that NTF OF showed a decreasing pattern. This demonstrated that our hypothesis was validated in different regions, and the elevation sampling method can resolve the observation biases and present more accurate results.
Sampling range
When we truncated the sampling range to 2100–3500m at Gaoligongshan where the samples were equidistantly collected along the sample lines (distance method), it was found that the original mid-elevation peak pattern (mid-peak pattern for OF, LPMP pattern for species number) changed to a decreasing pattern for the elevation sampling method. Previous studies on truncation and scale effects on the elevational distribution of species have been carried out. Truncating the low-altitude range of the studied region led to the changes of the elevational distribution of species from the mid-peak pattern to a decreasing pattern [18]. When the elevational gradient was entirely surveyed, the pattern was hump-shaped, changing eventually to a decreasing pattern as the scale of extent diminished. Likewise, the OF at the same altitude range of Cangshan (2100–3500 meters) was also a decreasing pattern. This result further supports the view that truncating the elevation gradient (i.e., insufficient sampling range) significantly affects the overall elevational distribution pattern observed.
Anthropogenic disturbance
Areas rich in biodiversity often overlap with areas of high human populations, and it’s generally accepted that human disturbance can affect the distribution of biodiversity [31–33]. Surprisingly the influence from human disturbance on species richness models has been long ignored. In recent years, some researchers have given this some attention, pointing out that human populations are generally based around low elevations, and therefore human disturbance is not evenly distributed across most elevations [34, 35].
The OF of NTF at Cangshan exhibited a decreasing pattern, while species number showed the LPMP pattern. The eastern slope of Cangshan below 2200m asl is occupied by villages and farms, in west slope of Cangshan Mountain, below 2400m asl is farmland. The Cangshan Nature Reserve not includes areas down to 2100–2300m, so that areas outside the reserve are affected by human disturbance to varying degrees [36]. When omitting the data collected in the range of 2100–2300m from Cangshan, we found both the OF and species number of NTF exhibited a decreasing pattern, which suggesting human disturbance affects the elevational richness pattern of NTF. The biodiversity in the low-altitude areas may have been artificially reduced due to human disturbances, thus creating the illusion of a mid-peak pattern. This may have been the reason why the species number of NTF at Cangshan showed a LPMP pattern when including the human-disturbed areas. Although we did not specifically quantify human disturbance in this study, our ability to alter the observed pattern by eliminating human disturbed sites highlights the importance of present and past human activities on patterns observed in nature.
Prospects and suggestions
When we used different indicators (OF and species number) to identify microbial biodiversity on the altitude gradient in this study, the same set of studies presented different results, it probably meant that our previous studies did not reflect the full picture of biodiversity. Johnathan et al. (2018) pointed out that because of multidimensional and scale-dependent characteristics of biodiversity, it would be better to describe its change from multiple perspectives [37]. Multidimensionality made the study of biodiversity at different time and different space more challenging than other variables in ecology [38]. In some studies, elevational diversity patterns presented by different indicators (species number, species density, evenness, biodiversity index) are different [12, 39, 40], thus the distribution patterns shown by different biodiversity indicators seemed to be interlaced, and different indicators showed different dimensions and different levels of biodiversity, to describe the biodiversity more fully from multiple dimensions needs more research and exploration.
Despite the viewpoints from Nogues et al. (2008) that the removal of high altitude areas had little effect on elevational richness pattern of species [18], the Three River Parallel Region in China is characterized by vast elevation span, climate and vegetation; the alpine mudstone beach and yearly snow-pack in the high-altitude areas may cause steep fall of biodiversity. In this study, the altitude range was not large enough to completely cover the whole range of “the Three Rivers Parallel Region” and to carry out the exploration of the impact on the elevational distribution in the high-altitude areas. Future research should also focus on the integrity of the altitude range and further extend the studied areas.
We also note that OF is frequently used in microbiological studies as an indicator of species density which was relatively less affected, but the large animals might be more affected if the number of species was used as an indicator, therefore, the species inconsistency which was in the studies on the elevational distribution may be related to sampling patterns. Of course, the environmental heterogeneity, caused by altitude, is more than the difference of temperature, precipitation and vertical area. In the future, we need to systematically carry out the research by integrating environment, biological groups, sampling patterns and data analysis to obtain the real situation of the elevational distribution of species, which is crucial to understand the forming mechanism, maintaining mechanism and large-scale distribution of microorganisms.
Based on our results, we believe the elevation interval method coupled with a rigorous sampling effort are best suited to richness studies of NTF and other taxon across environmental gradients. The results in this study suggested that future studies should address the sample-laying patterns and ensure not only the sampling evenness at each altitude, but also the consistency of the altitude range between the studied areas. A rarefaction curve should be employed to determine the rationality of the sampling, wherever possible, and at the same time, attention should also be paid to the impact of human disturbance along any environmental gradient measured.