4.1 Macroinvertebrate assembles
Forty-six taxa of aquatic macroinvertebrates belonging to 41 genera and 25 families were collected in hilly ponds of Liangping District in late spring. They were dominated by Diptera, but less Crustacea, Ephemeroptera and Trichoptera. Compared with other ponds, the taxa of macroinvertebrates were less, and the composition of the assemblages was different. For example, a survey of macroinvertebrate communities in 51 alpine lakes and ponds in Spain identified 84 taxa with an average richness of 18.8 (Garcia-Criado, Martinez-Sanz, Valladares, & Fernandez-Alaez, 2017). A total of 228 taxa of macroinvertebrates belonging to 68 families and 21 orders were found in 95 urban and rural ponds in the UK, among which Coleoptera was dominant (Hill, Heino, White, Ryves, & Wood, 2019). Based on the investigation of 30 urban and rural ponds in the UK, 192 taxa of 14 orders were collected, among which Coleoptera was dominant (Thornhill, Batty, Death, Friberg, & Ledger, 2017). The taxa collected in this experiment were less, which might be due to the high concentration of nutrients in the ponds. The diversity of aquatic macroinvertebrates was usually negatively correlated with the concentration of nutrients. We found that the concentration of TN was higher than 2 mg/L, and the concentration of TP was higher than 0.2 mg/L in most ponds, which meant on the state of eutrophication. Figure 5(a) also showed that a large number of invertebrates were inhibited by nitrogen. In this experiment, the major function of most ponds was aquaculture. The management behavior of managers, such as feeding and disinfection, would also have a strong interference on the aquatic food chain, thus reducing its biodiversity. Therefore, the results of this experiment identified a subset of aquatic macroinvertebrate assemblages in hilly region, and also showed that the value of the regional biodiversity was damaged. It had great potential to improve the habitat quality and ecosystem services of the ponds.
4.2 Spatial pattern
With the increase of physical distance, the limitation of taxa diffusion would increase, which might form spatial correlates (Legendre and Legendre, 1998). Therefore, we usually assumed that habitats with closer distance had more similar communities than habitats that were far apart, and the intensity of their impact depended on the characteristics of individual diffusion ability (Razeng et al., 2016). For the study of freshwater organisms, the study area might be a single basin or basins. It was generally believed that biological diffusion was more likely to occur within a basin than among basins (Jani Heino et al., 2015). Therefore, the spatial correlates of species are more likely to occur among basins. Aquatic assemblages can be affected by both spatial and environmental variables. However, it is not clear at what spatial scale, spatial correlates is more likely to occur. It is generally believed that larger spatial scales are more prone to spatial correlates. Based on the investigation of aquatic organisms in three basins in Finland with a total area of 63609 km2, it found that the aquatic communities in different basins were mainly determined by the environmental variables and basin effects (Jani Heino, Soininen, Alahuhta, Lappalainen, & Virtanen, 2017). Based on the investigation of aquatic insects in the ponds of Stockholm, Sweden, which covers an area of 2700 km2, little significant correlation was found between spatial distribution and diversity of aquatic insect (J. Heino et al., 2017). However, some studies had shown that the scale of study area did not necessarily correlate with spatial correlates. For example, the spatial correlates of taxa in the ponds of Oxford County was reported which study area was 2608 km2 (Briers & Biggs, 2005). However, in the survey of 51 alpine lakes and ponds in Castilla y León of Spain with an administrative area of 94223 km2, no spatial correlates of taxa was reported in most areas (Garcia-Criado et al., 2017). This supports the hypothesis that a common typology can be applied to a group of aquatic ecosystem with irregular distribution in a large-scale region. The investigation area of this experiment was 1892.13 km2, and the spatial correlates of taxa were not obvious. There are two possible reasons for this phenomenon. One is that compared with other spatial correlates studies, the scale of the study area is smaller, the geographical barrier of species among basins is smaller, and it is easy for macroinvertebrates to diffusion. Although geographical factors were the main factors controlling the composition structure of macroinvertebrates in wetlands, but the differences among basins in small-scale region were negligible (Batzer & Ruhi, 2013). Second, the altitude of the study area is low. Biogeographical effects (among basins), such as historical effects and climate stress, have little impact on aquatic communities in lowland areas. In lowland areas, there might be similar communities in different basins (Hoeinghaus, Winemiller, & Birnbaum, 2007).
4.3 Impact of environmental and spatial variables on the assembles
In large-scale research, spatial correlation is more likely to occur. However, in small-scale and scattered wetlands, the spatial variation of aquatic macroinvertebrate community was mostly explained by local environmental variables (Tornwall, Pitt, Brown, Hawley-Howard, & Baldwin, 2020). This experiment involved area of 1892.13 km2. The differences of altitude and surrounding habitat led to the differences of habitat conditions among sampling sites. Meanwhile, there were different environmental factors affecting the aquatic macroinvertebrate community in different basins. Nutrients had a certain influence on the distribution of macroinvertebrates in ponds (Smith, Vaala, & Dingfelder, 2003). It was widely recognized that high concentrations of nutrients could reduce the richness and diversity of aquatic macroinvertebrates (Thornhill et al., 2017). In particular, species that were sensitive to high concentration of nutrients, such as Culicidae sp., Spercheus emarginatus and Diplonychus esakii, decreased with the increasing concentration of nutrients. Dissolved oxygen is another factor affecting the distribution of aquatic macroinvertebrates. For different species, the influence of DO is different. Studies had shown that DO was an important factor of snail distribution, with positive correlation (Vansomeren, 1946) and negative correlation (Hurley, Hearnden, & Kay, 1995). Dissolved oxygen may have a great impact on dragonflies. Larvae of dragonfly mainly relied on DO to breathe (Griffiths C, Day J & Picker M, 2015). In addition, higher diversity of water beetles in ponds was associated with lower dissolved oxygen, which might indicate the presence of carnivorous vertebrates (Deacon, Samways, & Pryke, 2018). In this paper, the difference with these studies was that DO was only significantly correlated with macroinvertebrate assemblagesin basin 1. Gastropods, Odonata and water beetles had little correlation with DO. Area has always been one of the important factors to aquatic organisms in ponds. The area of ponds can affect the microhabitat structure and number. Based on the traditional island biogeography (MacArthur and Wilson 1967), it could be concluded that high quality and large ponds had higher biodiversity, including biodiversity of invertebrates. According to the habitat diversity hypothesis, the impact of area on species richness is mainly realized through biodiversity. The larger the area, the greater the species diversity (Ricklefs & Lovette, 1999). The habitats with large area, permanent inundation and alkalinity tended to have high biodiversity (Hoverman et al., 2011). However, some studies had shown that a group of small ponds was a key contributor to the biodiversity of regional invertebrates (Boix et al., 2012; Scheffer et al., 2006; Wood, Greenwood, Barker, & Gunn, 2001). The decrease of invertebrate biodiversity in the larger ponds might be due to the increase of fish and waterfowl in the ecosystem, which led to the exclusion of some invertebrates and the decrease of plant complexity (Schilling, Loftin, & Huryn, 2009). Or several ponds could increase the number of niche (P. Williams et al., 2004). Study showed that when the area gradient was narrow, the correlation between area and macroinvertebrate community might not be significant (Moraes, Stenert, Rolon, & Maltchik, 2014). However, it was interesting that the gradient of pond area in basin 2 was the narrowest, but the significant correlation between area and species only occurred in basin 2 in this paper. The gradient of altitude among ponds in basin 2 was 501 m, which was larger than the other two basins. There was a significant correlation between species and altitude in basin 2. This proves that there is a significant correlation between altitude and assemblages in low altitude areas. In addition to the above factors, temperature also has a significant impact on the spatial distribution of invertebrates. Among all organisms of wetland, invertebrates might be one of the animals most affected by temperature, because as ectotherms, their life cycle and growth rate were controlled by temperature (Kingsolver et al., 2011).
Another environmental factors as pH usually had a significant impact on the invertebrate assemblagesin ponds (da Rocha et al., 2016; Epele & Miserendino, 2016; Mabidi et al., 2017), but the relationship between them was less investigated in field (Spyra, 2017). Variation of pH could cause changes in food supply and affect the growth, development and survival of species indirectly (Friday, 1987). Different aquatic macroinvertebrates have different sensitive degree to pH. Larvae of dragonfly were sensitive to different pH gradients, as Anax had a wide range of pH (Jooste, Samways, & Deacon, 2020). One of the environmental problems faced by invertebrates in ponds is acidification. In the past decades, the negative effects of acidification on function and diversity of ecosystem had become more and more obvious (Guerold et al., 2000). Acidification induced by human had a greater impact on snails than natural acidification (Petrin, Laudon, & Malmqvist, 2007). Mollusca were the most sensitive species to acidification, so they were greatly affected by pH (Skowronska-Ochmann, Cuber, & Lewin, 2012; Sowa, Krodkiewska, Halabowski, & Lewin, 2019). In the study of forest ponds, 14 gastropods were collected in alkaline ponds (pH > 7.2), 18 gastropods were collected in neutral ponds (pH 6.8–7.2), 18 gastropods were collected in acidic ponds (pH 6 ≤ pH < 6.6), and 8 gastropods were collected in acidic pond system (pH 4.4-6) (Spyra, 2017). When the pH value of water was lower than 5.2, gastropods might not survive (Singh & Agrawal, 2008). There was no reference value for the pH tolerance range of gastropods, and it was considered that 5.5–9.5 was the adaptive range of gastropods (Spyra, 2017).
Three aspects show the effect of pH on invertebrates in ponds as follows. First, a large number of studies had shown that the higher pH value was, the greater taxa richness of invertebrates in ponds was (J. Heino, 2000; Kochjarova et al., 2017; McDevitt-Galles, Calhoun, & Johnson, 2018; Nicolet et al., 2004). For example, the abundance of Aeshnidae, Coenagrionidae, Corixidae and Gerridae was higher in the sampling sites with higher conductivity and pH value (Dalu & Chauke, 2020). This might be due to the fact that acidity could increase the toxicity level of some metals (such as Al, Cd, Pb, Zn), thus directly or indirectly affecting macroinvertebrates (Herrmann et al., 1993). Moreover, under alkaline conditions, generalists, such as Hemiptera, were more competitive than obligate species (Jooste et al., 2020). Secondly, some studies suggested that the functional diversity of invertebrates was smaller under high pH conditions (Interagency Freshwater Group, 2015). Related studies were mainly focused on water beetles (Arnott, Jackson, & Alarie, 2006; Roth, Zoder, Zaman, Thorn, & Schmidl, 2020) and Oligochaeta (Krodkiewska, Strzelec, & Spyra, 2016). It might be for the reason that under natural conditions, lower pH values were associated with higher residues and humus of vegetation (Vuorenmaa, Forsius, & Mannio, 2006). The accumulation of detritus also increased the diversity of habitat structure, thus increasing species richness (Schmidl, J, 2003). Thirdly, some studies found that pH value had no significant effect on density of invertebrates (Simpson, Bode, & Colquhoun, 1985; Winterbourn & Collier, 1987). Therefore, under certain conditions, pH will have an impact on aquatic invertebrates, and the impact on different species is different. Some invertebrates such as Odonata and aquatic beetles may prefer alkaline water, while some invertebrates such as aquatic beetles and Oligochaeta may prefer acidic water. In this paper, there was a significant positive correlation between pH and Spercheus emarginatus which belonged to aquatic beetles, and a significant negative correlation between pH and Diplonychus esakii which belonged to aquatic beetles.
According to the theory of island biogeography, biological assemblages of ponds should affected by the size and isolation degree (Holland & Jain, 1981; Ripley & Simovich, 2009). Island size could affect the survival rate and available niche, while isolation affected the migration rate (MacArthur RH and Wilson EO, 1967). The effect of isolation on biological communities was related to the migration ability of organisms among habitats (Hanski, 1999). Species with strong migration ability are less likely to species extinction. Aquatic macroinvertebrates can migrate from one pond to another by active or passive diffusion, thus increasing species exchange among ponds. Meanwhile, not all species responded to habitat size and area (Scheffer et al., 2006). In recent years, little attention had been paid to the index of isolation for ponds (Brooks & Colburn, 2012). Some studies had also shown that the richness of aquatic or terrestrial invertebrates was not related to isolation of habitat (Brooks & Colburn, 2012; Jonsson, Yeates, & Wardle, 2009; Moraes et al., 2014; Scheffer et al., 2006). However, other studies had shown that the increase of isolation among ecosystems could reduce the migration rate and increase the risk of species extinction (MacArthur RH and Wilson EO, 1967). Isolation was an important factor affecting the distribution of gastropods (Bronmark, 1985) and the migration pattern of predatory aquatic insects (Wilcox, 2001). Briers and Biggs believed that the isolation degree of ponds had a significant impact on invertebrate community, and the invertebrate community structure among adjacent sampling sites was more similar than that among distant ponds (Briers & Biggs, 2005). Significant correlates between isolation degree and species assemblageswere found in both basin 1 and basin 2 which was in line with previous studies.
4.4 Implication for biodiversity conservation of ponds
Different aquatic ecosystems support different community structures of aquatic macroinvertebrates. The physical and chemical characteristics of water, such as pH, DO and transparency, are important factors affecting the community structure of aquatic macroinvertebrates. At the same time, due to the regularity of regional water quality, regional aquatic macroinvertebrates usually show relevant regularity. So we can understand the characteristics of regional biodiversity, the scale and species to be protected. To a certain extent, artificial ponds of hilly area in China maintain the scale of local aquatic species, expands the habitat area, and improves the functional connectivity of most ponds. As a “stepping stone” of habitat, it provides convenience for the migration and diffusion of aquatic organisms. However, hilly ponds are also faced with over utilization and serious agricultural non-point source pollution. In addition to the establishment of statutory reserves, we need to shift the unreasonable utilization of ponds to the sustainable development of biodiversity resources desperately. The cost-effectiveness of protection management must be considered, and protection decisions also be constrained by multiple conflicts of interest. Therefore, we need to conserve the habitat and biodiversity of ponds from the aspects of landscape scale, habitat conditions and industrial structure etc.. In terms of landscape scale, we should focus on the landscape level of ponds rather than single pond (Briggs, Pryke, Samways, & Conlong, 2019; Hill et al., 2018; Thornhill et al., 2017). In terms of habitat conditions of ponds, the restoration of ponds habitat should pay attention to nutrients (such as TN, NH4+), distribution pattern (such as isolation), temperature and climate (such as altitude), habitat structure (such as area). At the same time, we should be alert to the loss of biodiversity caused by acidification of human activities. In China, a large number of artificial ponds are permanent, and they may become temporary wetlands for no artificial management. As a part of the protection and management strategy, it was encouraged to maintain the pond network with different length of hydrological cycle and environmental characteristics (Hill et al., 2017). In terms of industrial structure, we can introduce more sustainable utilization modes into the production and utilization of ponds, increase the economic output of ponds, and realize biodiversity conservation with low-cost.