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Sep 7, 2017 - 4Graduate School of Science, Kobe University, 1-1 Rokkodai, ... River Planning and Management Division, Department of Public Works, ...
Examination of the link between life stages uncovered the mechanisms by which habitat characteristics affect odonates NORIKO IWAI,1,  MUNEMITSU AKASAKA,1 TAKU KADOYA,2 SHINYA ISHIDA,2,5 TAKASHI AOKI,3 SHINSUKE HIGUCHI,4 AND NORIKO TAKAMURA2 1

The Institute of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai-cho, Fuchu, Tokyo 183-8509 Japan 2 Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506 Japan 3 Sumashofu High School, 1-5-5 Nishiochiai, Suma-ku, Kobe 654-0155 Japan 4 Graduate School of Science, Kobe University, 1-1 Rokkodai, Nada-ku, Kobe 657-8501 Japan

Citation: Iwai, N., M. Akasaka, T. Kadoya, S. Ishida, T. Aoki, S. Higuchi, and N. Takamura. 2017. Examination of the link between life stages uncovered the mechanisms by which habitat characteristics affect odonates. Ecosphere 8(9): e01930. 10.1002/ecs2.1930

Abstract. The larval and adult stages of amphibious animals are affected by both aquatic and terrestrial habitat characteristics, and each stage also affects the other. However, this link between life stages has been largely overlooked in previous studies. We examined the effect of aquatic and terrestrial habitat characteristics on the diversity of larval and adult odonates, taking into account the link between the two life stages. Species diversity of adult and larval odonates and aquatic plants, as well as patterns of land use, was investigated in 63 irrigation ponds. We created structural equation models, with paths from land use and aquatic plants characteristics to larval and adult stages of odonates, as well as between the two stages, and chose the best model based on the lowest Akaike information criterion. Adult odonates, but not larvae, were affected by aquatic and terrestrial habitat characteristics, suggesting that the former is the key stage for odonate communities. We observed a positive relationship between the diversity of aquatic plants and larval odonates, but this was in fact due to the effects of aquatic plants on adults, which carried over to the larval stage. Our study showed that a consideration of the link between life stages is crucial for a complete understanding of the relationship between habitat characteristics and amphibious animal populations. Key words: amphibious animal; aquatic plant; carryover effect; damselfly; dragonfly; irrigation pond; land use; structure equation model. Received 18 January 2017; revised 5 June 2017; accepted 28 June 2017. Corresponding Editor: Andrew C. McCall. Copyright: © 2017 Iwai et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Present address: River Planning and Management Division, Department of Public Works, Niigata Prefecture, 4-1

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Shinko-cho, Chuo-ku, Niigata 950-8570 Japan.   E-mail: [email protected]

INTRODUCTION

isolate the most important factors contributing to the persistence of such species’ populations. When the target species has a complex life cycle (Wilbur 1980), such as an amphibious animal with an aquatic larval stage and a terrestrial adult stage, the life stage’s performances are interconnected (Tarvin et al. 2015), and the identification of factors that influence population health requires consideration of this fact. As larvae develop into adults, their performance,

Boundaries between aquatic and terrestrial ecosystems are known to be important habitats for many wildlife species (Sabo et al. 2005). Because the animals inhabiting these boundary areas are affected by multiple characteristics of both the aquatic and terrestrial ecosystems (Denoel and Ficetola 2008, Ma et al. 2010, Goertzen and Suhling 2013), it is often difficult to ❖ www.esajournals.org

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observed relationships when identifying factors that influence population. For example, if data reveal a relationship between land use and adult odonate performance, such a relationship may not be explained by a direct effect of land use on adult odonates, but by an indirect effect via the larval stage: Land use may, for instance, affect the diversity of aquatic plants, which then affects the diversity of larval odonates, the effect of which in turn is carried over into the adult stage. In the present study, we examined the effect of aquatic and terrestrial habitat characteristics on the diversity of larval and adult odonates, while also considering the link between the two life stages. We built structural equation models (SEM) to analyze the influences and interactions of these factors. Using the selected models, we will show how including the link between the two life stages could reveal the actual paths of effects between habitat characteristics and different life stages of odonates.

reflecting the conditions of the aquatic habitat, will directly affect their performance in the later (adult) stage (Anholt 1991, Pechenik 2006, Earl and Semlitsch 2013)—while adult performance, reflecting terrestrial environmental conditions— will be carried over to the next generation (Richter-Boix et al. 2014). Thus, in both life stages, amphibious animals will be directly affected by aquatic and terrestrial habitat characteristics and indirectly affected through the link with the other life stage. When identifying factors that influence population health, this link must be taken into consideration as it complicates the relationship between habitat characteristics and population performance. However, the carryover effects between life stages have gained attention only recently (Pechenik et al. 1998, Stoks and rdoba-Aguilar 2012, Van Allen and Rudolf Co 2013) and have thus far not been included well in studies of the relationship between habitat characteristics and amphibious animal populations. Odonates are one such amphibious clade, using both aquatic and terrestrial ecosystems (Corbet 1980). They are declining worldwide because of the deterioration of habitat (Kalkman et al. 2008, Clausnitzer et al. 2009), while this taxon is important because it reflects the quality of both aquatic and terrestrial ecosystems, being a good indicator (Briers and Biggs 2003). A number of studies have examined factors that influence the performance of odonate populations. For example, the diversity of adult odonates is affected by terrestrial environmental factors such as land use practices (Samways and Steytler 1996) and forest disturbance (Dolny et al. 2012). Adult odonates are also affected by aquatic environmental factors, such as diversity of aquatic plants (Foote and Hornung 2005, Hassall et al. 2011), because odonates depend on aquatic plants for oviposition (Goertzen and Suhling 2013). Larval odonates are similarly affected by both aquatic and terrestrial factors, such as the diversity and structure of aquatic plants in their habitat (Corbet 1980, Heino 2002), elements that are also often influenced by terrestrial land use (Declerck et al. 2006, Akasaka et al. 2010). Previous studies, however, have treated either of adult or larval stages, or even though considering both, they treated two stages independently (Raebel et al. 2012) or only with unidirectional relationship (Anholt 1991). This oversight may have led to misunderstanding of the mechanisms underlying the ❖ www.esajournals.org

METHODS We conducted field survey in 63 irrigation ponds in the southern part of Hyogo Prefecture in western Japan (34°510 N, 135°030 E) in 2006–2008 (Fig. 1). The ponds were intensively created before the 1910s to overcome shortages of water for rice cultivation (Uchida 2003) and currently used only for water storage and not for other commercial purpose (e.g., fish farming). Pond surface areas ranged from 0.1 to 3.7 ha (mean  SD: 0.9  0.7 ha), and the distance between ponds ranged from 100 m to 4260 m (mean  SD: 1260  1170 m). More information of the study ponds is in Akasaka and Takamura (2012). We measured important environmental factors affecting the diversity (species richness) of odonates in both life stages: land use for terrestrial habitats (Samways and Steytler 1996, Declerck et al. 2006, Akasaka et al. 2010) and diversity (species richness) of aquatic plants in aquatic habitats (Corbet 1980, Heino 2002, Foote and Hornung 2005, Hassall et al. 2011). There was a wide variety of land use and a range of aquatic plant diversity among the different ponds, providing an excellent natural experimental system for examining the effects of these factors on odonates. Surveys of odonate adults (Oa) were conducted between October 2006 and September 2007 (31 2

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Fig. 1. Map of irrigation ponds located in Hyogo Prefecture, Japan.

around the perimeter of each pond on average. When determining the sampling place, we described the environments according to vegetation (emergent, floating, submerged, terrestrial, none), litter (aquatic plant origin, terrestrial plant origin, none), and sediment (sand, rock), and carefully chose different combinations of the categories in order to include all the species of Ol inhabiting different microhabitats. All the Ol thus collected were identified to species level. Aquatic plants (Ap) surveys were conducted at the approximate peak of plant biomass (August and September) in 2006 and 2007. We used boats and visually checked species of Ap over each pond. We divided land use into six categories: freshwater, broad-leaved forest, paddy field, farmland, grassland, and urban area. We used digital land use maps and a geographical information system (ArcGIS 9.2; ESRI, Redlands, California, USA) to determine the percentage cover of the land use types. Details in determining land use percentages were in Akasaka et al. (2010). Because the sum of land use rates for the six categories was 1, and the proportion of broad-leaved forest showed relatively high correlation with the proportions of other categories (with urban area, r = 0.6; and with paddy field, r = 0.6), we excluded the category of broad-leaved forest from the analysis. We chose the extent of land

ponds), or between October 2007 and September 2008 (32 ponds). We surveyed each pond for six times during the period. The survey time was chosen so as to cover spring, summer, and autumn species (Corbet 1999). Census route was set along whole perimeter of each pond to find as many individuals as possible. The survey speed was set within 15–30 m/min, which resulted in spending proportional efforts on each pond according to its size. The species of odonates visually found from the route were all recorded. When species was not apparent from the visual survey, individuals were captured and identified. The identification was done within the length of net (3.6 m) from the census route. All the surveys were conducted by the same person (T. Aoki). Odonate larvae (Ol) surveys were conducted twice in each pond, once in the periods April– May 2007 and once in May–June 2007 (31 ponds), or once in November–December 2007 and once May–June 2008 (32 ponds). This survey time was chosen so as to cover two groups of odonates: one that overwinters as larvae and the other that overwinters as adult or egg. We placed 0.9 9 0.9 9 0.45 m quadrats and captured Ol by thoroughly dipnetting until no more larvae were found from vegetation as well as from sediment. The number of quadrats was determined according to the pond size and was placed every 60 m ❖ www.esajournals.org

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existed, we calculated Moran’s I in the residual of Oa at multiple distance classes from 200 to 1000 m at intervals of 50 m.

use that was most strongly correlated with changes in odonate diversity by buffer analysis (Appendix S1), and the distance was 250 m from pond edges (Appendix S1: Fig. S1). Structural equation model allows tests of multivariate causation with a visual path diagram displaying model components and direct and indirect causal pathways (Shipley 1999) and has been used in several recent works for evaluating hypotheses in ecology (Austin 2007, Joseph et al. 2016). We constructed a SEM to separately examine the direct and indirect effects of aquatic and terrestrial environments on odonates in adult and larval stages (Fig. 2). These models contain direct effect paths from land use to Oa, Ol, and Ap, which can then affect Oa and Ol. Ol and Oa are mutually influencing. Models were analyzed using Amos software (ver. 20.0.0; IBM, Armonk, New York, USA). Models with all possible combinations of effect paths were examined using the exploratory model selection function in Amos, and the model with the lowest Akaike information criterion was selected. Selected model was examined its fit to the data by chi-square statistic and goodness-of-fit index (GFI). Significance of chi-square test indicates rejection of the model (Vile et al. 2006), and GFI > 0.95 indicates wellfitting models while GFI > 0.90 indicates an acceptable fit (Schermelleh-Engel et al. 2003). Root mean square error of approximation (RMSEA), the other indices of fit that are often used in SEM, was also assessed. Good models have a RMSEA < 0.05 (Vile et al. 2006). In order to examine whether spatial autocorrelation

RESULTS We found between four and 30 species of adult odonates, between 0 and 16 species of larval odonates, and between 0 and 22 species of aquatic plants per pond (Appendix S2: Tables S1 and S2). In the SEM analysis, the best model fit the data reasonably well (v2 = 12.3, P = 0.506; GFI = 0.953; RMSEA < 0.001; Fig. 3). Effect paths from freshwater, paddy field, and urban area were included as land use variables affecting Oa diversity. Standardized coefficients for each variable were negative, with the largest effects from paddy field (0.50) and urban area (0.46). Ap diversity was affected positively by farmland (0.24) and negatively by paddy field (0.18) and urban area (0.24). Oa diversity was positively affected by Ap (0.37). The path from Oa to Ol was positive (0.77), but that from Ol to Oa was not included. Ol was not directly affected by Ap, but there was an indirect effect with a size of 0.37 9 0.77 = 0.28. Land use also indirectly affected Oa diversity. Indirect effects on Oa via Ap were seen from paddy field (0.18 9 0.37 = 0.07), urban area (0.24 9 0.37 = 0.09), and farmland (0.24 9 0.37 = 0.09). These values were relatively small compared to direct effects from each land use variable. Ol was not directly affected by any of the land use categories. The Moran’s I values in the residuals of Oa were from 0.32 to 0.15, and no significant spatial autocorrelation was detected at any distance classes.

Fig. 2. Full model used for structural equation model analysis. Abbreviations are WAT, freshwater; PAD, paddy field; FAR, farmland; GRA, grassland; URB, urban area; Ap, aquatic plants; Oa, odonate adults; Ol, odonate larvae.

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Fig. 3. The selected structural equation model with standardized coefficients. For the definitions of the abbreviations in this figure, refer the caption of Figure 2.

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DISCUSSION

adults than to the larval stage. One of the approaches to make environments more favorable to adult odonates is to increase the diversity of aquatic plants, as stated above. The important thing is that, when increasing diversity of aquatic plants, we should be aware that the aim is to increase them for adult stage, rather than for larvae. With this in mind, in cases where it is not feasible to increase aquatic plant life, creating man-made structures appropriate for oviposition could be an effective alternative conservation strategy. Our models show that changes in land use patterns also affect odonate communities, with an effect size at least as great as that of aquatic plants. According to these models, a decrease in the amount of habitat used as paddy fields and/ or urban areas will lead to an increase in diversity of adult odonates. Previous research has found a positive relationship between paddy field prevalence and adult odonate communities (Kadoya et al. 2009). Our contrary result may reflect the negative relationship between the amount of land used as paddy fields and the extent of forest area (r = 0.58). As forests provide an essential habitat for adult odonates (Dolny et al. 2012), an increase in the proportion of paddy fields, with a corresponding decrease in forest area, might have a negative effect on adult diversity. The explanation for the negative relationship between the extent of urban area and odonate population is straightforward: Urban areas decrease the amount of available habitat for adult odonates, and often support only generalist species, leading to lower diversity (McKinney 2008, Kadoya et al. 2011, Goertzen and Suhling 2013). In addition to these direct effects on adult odonates, patterns of land use also have indirect effects through their effect on aquatic plants. However, in our observations, indirect effect paths were not as powerful as direct ones. Thus, these indirect pathways are less efficient tools for influencing odonate communities. When land use pattern has favorable effects (both direct and indirect) on adult odonates, these positive effects will be carried over to the larval stage, and odonate communities will be in a good condition. Other variables, such as the physical characteristics of ponds or topographical conditions, could also be added to our models. However, adding more variables increases the complexity of the

Our results showed that adult, but not larval, odonates were directly affected by aquatic and terrestrial habitat characteristics and that larval odonate populations were only affected by the characteristics of adult populations. This suggests that adulthood is the key stage for the odonate communities in this study: Greater diversity of adults leads to increased diversity in aquatic larvae. The diversity of adult odonates that used a given pond largely determined the diversity of larvae therein, and characteristics of the aquatic environment seemed not to be a limiting factor for larval odonates in the study area. By considering the link between the two life stages, we achieved a better understanding of the mechanisms underlying the relationship between habitat characteristics and Odonata communities. For example, aquatic plants have been known to have a positive relationship with adult (Bernath et al. 2002, Gibbons et al. 2002, Kadoya et al. 2004) and larval odonate populations (Hinden et al. 2005, Carchini et al. 2007, Hassall et al. 2011, Goertzen and Suhling 2013). These positive relationships were thought to be caused by adults using aquatic plants as structures for successful oviposition (Corbet 1980) and larvae using aquatic plants as their habitat (Corbet 1980, Heino 2002). In our study, we did observe a positive effect on the diversity of aquatic plants and larval odonates. However, we determined that this effect could be explained by the strong positive relationship between aquatic plants and adult odonates, which depend on plants for oviposition, with this effect being carried over to subsequent generations of larvae. It is possible that this relationship between life stages also explains the effects observed in previous studies; it is thus essential to consider the link between life stages to correctly understand the pathways of the effects of habitat characteristics on amphibious animals. Creating models with links between life stages allowed us to determine which life stage drives changes in odonate communities, and the factors affecting that life stage. This approach should prove especially effective in informing conservation strategies for amphibious animals. For example, our results clearly showed that, to increase diversity of odonate communities, it would be more effective to create environments favorable to ❖ www.esajournals.org

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models and may cause difficulty in interpreting results. It is important to choose appropriate factors according to the questions being asked. In addition, we treated odonate communities as a whole and did not consider different ecological groups among them. For example, our data included those species that are strongly associated with aquatic plants as well as those that are not. This may lead to different conclusion with different data set in other areas. It would be interesting to explore how the relative importance of aquatic and terrestrial characteristics on two life stages would differ among ecological groups in future. Although we used simple models, our study succeeded in showing the importance of the link between different life stages in the relationship between habitat characteristics and populations of amphibious animals. Our approach, considering link between life stages, is applicable to any species with a complex life cycle that inhabits boundary areas between different ecosystems. This approach will be valuable in future studies for revealing the effects of habitat characteristics and the mechanisms by which they act on populations and communities of such animals.

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ACKNOWLEDGMENTS We would like to thank Ms. Megumi Nakagawa for field assistance and Dr. Yasuro Kadono for advice. This research was supported by the Environment Research and Technology Development Fund (S-9) of the Ministry of the Environment of Japan, and partly supported by JSPS KAKENHI Grant Number JP 17K17706 and 17K15056.

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SUPPORTING INFORMATION Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ecs2. 1930/full

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