The Use of Highly Diverse Clades As A Surrogate For Habitat Integrity Analysis: A Practical Tool For Rapid Assessments

Human activities have impacted many different habitat types on Earth, and there is a requirement for tools with which to accurately assess the level of damage incurred by ecosystems. For environmental analyses and monitoring, rapid stream assessment techniques emphasize geomorphological characteristics, biological potential, and habitat integrity characteristics. Using the principles and concepts of aquatic biology and ecology, we determined whether the visual-based habitat evaluation score is related to Odonata species diversity at different taxonomic levels. We hypothesized that habitat assessment is correlated positively with the local diversity of one Odonata taxonomic group. We found that the abundance, species richness, and diversity of Argia, one of the most locally diverse genera in southeastern Mexico, are positively correlated with habitat integrity scores. High richness (of up to eight species per site) corresponds to high integrity scores. Simultaneously, habitat integrity scores increase 23.51 times when Argia diversity (surface area) increases. We discuss the possible advantages of using a diverse Odonata clade (Argia) as a surrogate for local habitat assessments. Long-term biomonitoring programs could be applied using this novel approach in this specic Neotropical area. This study is framed within the focus of biodiversity and ecosystem functioning (BEF), however, it must be tested with other indices and a reliable and consistent relationship must be veried between diverse clades and environmental assessment scores. whether one taxonomic group can suciently explain habitat integrity to be of utility as a surrogate for rapid habitat assessment. We hypothesized that habitat assessment will correlate positively with a diverse clade, particularly the genus Argia because most of these species are typically specialists and thus sensitive to environmental quality (Šigutová et al., 2019), and could therefore be used as an indicator of habitat integrity in this specic area. We then compared the relationship using the information derived from General Linear Models (GLM). This comparison allows the discussion of techniques that attempt to correlate odonates diversity—specically Argia diversity— and habitat quality for local environmental assessments. Below, we discuss the possible use of Argia diversity for local long-term biomonitoring programs in tropical regions. However, we open the debate regarding the value of focusing on studying diverse clades as practical proxies of habitat integrity and verify whether there is a reliable and consistent relationship with other taxa and environmental indices, in the Neotropical region.


Introduction
Ecosystems, both aquatic and terrestrial, face an unprecedented environmental crisis. The high number of extreme meteorological events (Luque et al., 2013), increased presence of chemicals with toxic effects on human health (Shen and Zuo, 2020) and loss of species (Dirzo et al. 2014) are three of the most critical challenges we currently face. Freshwater habitats in particular represent one of the world's most threatened ecosystems (Dudgeon et al., 2006;Voß & Schäfer;. For example, rivers ecosystems are increasingly affected by various factors as a result of the development of human activity (Valero et al., 2015). Maintenance of safe freshwater resources is therefore an urgent requirement worldwide, and there is a general trend towards examining threats over a broad range of scales, local to global, from both social and biological perspectives (Vörösmarty et  On the other hand, habitat assessment has been de ned as evaluating the surrounding physical habitat structure that in uences the quality of the water resource and the resident aquatic community (Barbour et al. 1996). An integral approach to assessing habitat structure includes evaluating substrate variety and quality, channel morphology, bank structure and riparian vegetation (Barbour et al., 1999). Rapid habitat assessments are often based on an observer rating the habitat integrity of the site by matching speci c habitat features (Hannaford et al., 1997). Habitat assessments are, therefore, an e cient method for the characterization of stream habitat In this context, we explore whether Odonata biodiversity can predict the habitat integrity. The objective in this study was to analyze the relationship between the Visual-Based Habitat Assessment Score (VBHAS; Barbour et al., 1999) and the parameters of abundance, species richness and diversity, at different taxonomic levels in streams of Neotropical basins. Speci cally, we tested whether one taxonomic group can su ciently explain habitat integrity to be of utility as a surrogate for rapid habitat assessment. We hypothesized that habitat assessment will correlate positively with a diverse clade, particularly the genus Argia because most of these species are typically specialists and thus sensitive to environmental quality (Šigutová et al., 2019), and could therefore be used as an indicator of habitat integrity in this speci c area. We then compared the relationship using the information derived from General Linear Models (GLM). This comparison allows the discussion of techniques that attempt to correlate odonates diversity-speci cally Argia diversityand habitat quality for local environmental assessments. Below, we discuss the possible use of Argia diversity for local long-term biomonitoring programs in tropical regions. However, we open the debate regarding the value of focusing on studying diverse clades as practical proxies of habitat integrity and verify whether there is a reliable and consistent relationship with other taxa and environmental indices, in the Neotropical region.

Study site
We carried out this study in three permanent basins, Cintalapa, Vado Ancho and Huixtla ( Figure 1 hs., when the streams were illuminated by sunlight. Once species identi cation was completed, the individuals were released at their corresponding sampling sites. Where taxonomic identi cation in the eld was not possible, each individual was preserved by placing in a cooler at 4 ºC for at least 10 min to decrease the metabolism, then injected with 99% acetone and immersed for 24 hours in 99% acetone in order to preserve the original color. We carried out identi cation in the eld and laboratory using taxonomic keys (Westfall & May, 1996;Förster 2001;Garrison et al., 2010a;2010b). Each identi ed specimen was subsequently compared with the species described for the state of Chiapas, according to González-Soriano and Paulson (2011).
Visual-Based Habitat Assessment Score (VBHAS) We carried out the analyses of habitat quality for each SU according to a VBHAS proposed by Barbour et al. (1999)  . Each unique feature was determined, and the scores were calculated as the sum of each value. A high score therefore re ects a better habitat condition. All parameters were evaluated and rated on a numerical scale of 0 to 20 (highest) for each SU. The ratings were then totaled and compared to a reference condition (according to Barbour et al., 1999; Supplementary Material Appendix 3) to provide a nal habitat ranking. Kolem-Jaa-a site located on the state limits between Chiapas and Tabasco-was used as a reference site with which to compare the SU because of its null anthropogenic impact status and location within the same ecoregion. Scores rise with increasing habitat quality, and descriptions of the physical parameters and relative criteria were included in the rating form (Alonso Eguía-Lis et al., 2013) in order to ensure consistency in the evaluation procedure. The judgment criteria for each of the habitat parameters were calibrated for the stream classes under study, with some modi cations applied on a regional basis. Each person was trained in the visual-based habitat assessment technique for the applicable region in order to give a particular score, after which the highest and lowest scores were eliminated, and the remaining estimations used to provide an average score for each SU.  In this preliminary rapid assessment study with Odonata, we found the following relationships: The GLM analysis showed a positive correlation between VBHAS and Argia species richness (S), with an estimated slope of 12.06±5.09 (AIC = 119.30, p = 0.04; Table 2, Figure 3a). For Coenagrionidae diversity (surface area), we found an estimated slope of + 20.03±9.36 (AIC = 120.11, p = 0.06; Table 2, Figure 3b) and, for Argia diversity (surface area), the estimated slope was 23.51±7.16 (AIC = 115.97, p > 0.01; Table 2, Figure 3c). For Odonata and Zygoptera, we did not nd any relationship with VBHAS for abundance, species richness, or diversity.

Discussion
As expected, our results indicate that a highly diverse clade approach can be used to predict the environmental integrity of the streams in this study site. There is a growing need to identify rapid and effective biological indicators for measuring environmental health and  ) found that the population size of Argia species decreased when areas of urbanization and deforestation increased. Consequently, the mixture of specialist and generalist species acted to conceal the relationship with VBHAS, which was evaluated at a higher taxonomic level (order).
Classical species diversity measures use species richness, heterogeneity or evenness; however, as Magurran (2004)  because some indices prioritize species richness over uniformity (or vice versa). As a result, communities could be ranked differently depending on the index applied (Hurlbert, 1971). According to Stirling and Wilsey (2001), species diversity should be measured using a compound statistical metric. Since traditional diversity indices cannot summarize species diversity, a composite statistical measure is required (Guisande et al., 2017). Our study includes an analysis of the total diversity, abundance and species richness of odonates at different taxonomic levels (order, sub-order, family, and genera) with a habitat integrity index (VBHAS). We found that Argia species richness and diversity both increase with increasing habitat integrity indices. This relationship means that analysis at the genus level could be more accurate than at higher taxonomic levels for this particular region.
Unfortunately, little is known regarding the life cycles, geographic distribution and tolerance to environmental change of many odonate species in this region. It is therefore di cult to relate the environmental factors that affect each life cycle stage to presence or absence in a particular site. For this reason, we found insu cient information for this speci c Neotropical region to compare our results with other indices; for example, the Odonata Habitat Index (Chovanec and Waringer, 2001)  With regard to our hypothesis, we suggested that habitat assessment will correlate positively with a diverse clade, particularly the speciose Argia genus, and therefore expected a positive relationship since most of these species are typically running water specialists and sensitive to environmental integrity. Moreover, since these species belong to the same clade, they must share a common evolutionary and colonization history in this speci c area. We found a robust positive relationship between VBHAS with Argia richness and diversity, regardless of geographic position (latitude, longitude, and elevation World, with its highest diversity found in our study area (Caesar & Wenzel, 2009). Our approach also differs in that we tested different taxonomic levels (from order to genera) as predictors of habitat integrity. Nevertheless, this approach must be tested with other quality indices and other highly diverse clades in order to determine its accuracy.

Conclusions
Odonata species are of value to the assessment of lotic habitat integrity, especially in Neotropical ecosystems. However, when we compare the results obtained from the analyses between the different diversity indices and the VBHA scores, the parameters of richness and diversity were signi cant for Argia species.
This study demonstrates that it is possible to monitor Argia species associated with environmental integrity, preserved environments, and degraded streams, and the results show that species richness and diversity are both positively related to the visual habitat integrity index (VBHAS) scores in this Neotropical zone. Argia diversity has the lowest AIC value of all analyzed models.
This monitoring method can be applied by local people with no specialized biological training. However, further eldwork is necessary before establishing monitoring protocols. More data are required through the collection of female specimens to develop a eld guide that helps the identi cation of specimens by local non-specialist monitors.
We recommend the use of diverse clades for evaluating environmental integrity in order to test our hypothesis. We strongly suggest using odonates and other taxa for rapid environmental evaluations in the Neotropical region.

Declarations
Ethics approval and consent to participate Not applicable

Consent for publication
Not applicable Availability of data and materials All data generated and analyzed during this study are included in this published article as supplementary information les.

Competing interests
The authors declare that they have no competing interests.