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Article

Linear Landscape Elements and Heteropteran Assemblages within Mediterranean Vineyard Agroecosystems

by
Natalia Rosas-Ramos
1,*,
Josep D. Asís
1,
Marta Goula
2,
Iván Ballester-Torres
3 and
Laura Baños-Picón
1
1
Departamento de Biología Animal (Área de Zoología), Universidad de Salamanca, 37007 Salamanca, Spain
2
Departament de Biologia Evolutiva, Ecologia i Ciències Ambientals and IRBIo, Universitat de Barcelona, 08028 Barcelona, Spain
3
Research Institute CIBIO (Centro Iberoamericano de la Biodiversidad), Universidad de Alicante, 03080 Alicante, Spain
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(19), 12435; https://doi.org/10.3390/su141912435
Submission received: 21 July 2022 / Revised: 22 September 2022 / Accepted: 27 September 2022 / Published: 29 September 2022
(This article belongs to the Special Issue Functional Traits as Indicators of Environmental and Ecosystem Changes)
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Abstract

:
In agricultural systems, linear habitat features and resource shifting over the season can shape insect communities. When evaluating insect assemblages, the use of trait-based approaches allows measuring of the functional component of diversity which, combined with a taxonomical perspective, may help to understand how environmental factors drive community structuring. In Mediterranean vineyard agroecosystems, we assessed Heteroptera communities to evaluate linear habitat type (hedgerow vs. grass strip) and seasonality drive assemblages from both a taxonomical and a trait-based perspective. Morphometric traits related to dispersal ability or microhabitat and resource use were measured. Heteroptera community composition varied from hedgerows to strips and also changed over the season. However, the taxonomical response was not as strong as the trait one. Trait composition of the omnivorous heteropteran community remained stable when compared to those of phytophagous and predatory heteropterans, which were more sensitive to the evaluated factors. Given that each linear habitat type supports communities with different trait compositions, we highlight the importance of preserving a variety of habitats to achieve a high functional diversity. We also emphasize the need to develop studies at different spatial scales that allow to better understand the significance of landscape elements on shaping insect assemblages across different climatic regions.

1. Introduction

Currently, we are witnesses to a worldwide reduction in biodiversity that has been suggested as leading to considerable species extinction rates in the upcoming decades, many of those species being insects [1,2]. Biodiversity loss not only means a reduction in species diversity, but also a reduction in functional diversity, both components sometimes exhibiting different patterns [3,4]. This constitutes an alarming situation, since the reduction of taxonomic and functional diversity has an impact on ecosystem functioning, on the provision of ecosystem services, and on human well-being [1,5,6,7]. Agricultural areas are the largest ecosystem of the planet and thus condition a meaningful array of worldwide biological diversity [8,9,10]. The expansion and intensification of agriculture and the resulting loss of natural and semi-natural habitats are among the main drivers of biodiversity decline, and the respective reduction of underlying services [1,11]. However, there is a significant variability in how different crops affect biodiversity. The vineyard is an ancient crop that comprises 7.3 million ha of land globally, most of them located in Mediterranean-type ecosystems that support high levels of biodiversity and species endemism [12,13,14]. Vineyard agroecosystems contribute significantly to the identity, culture, economy, and biodiversity of many regions worldwide, but despite their significance they have received scarce attention from ecologists and conservationists, and little is known about biodiversity dynamics in these agroecosystems [15,16,17,18].
Due to their specific characteristics, vineyard agroecosystems are of particular interest in terms of conservation [15,16,19]. A noteworthy feature of vineyards is that they are usually grown in mountain environments and cultivated on steep slopes [13], which favor the maintenance of non-cropped areas. Within agricultural landscapes, and particularly in vineyards, ecological infrastructures and non-cropped linear habitats such as hedgerows or grass strips operate as reservoirs of biodiversity, promoting the presence of different taxonomic and functional groups that can spill over to other cropped and non-cropped habitats across the landscape [8,11,20,21,22,23,24,25,26,27]. Non-cropped linear habitats constitute more suitable habitats than arable lands given the variety of resources they provide, including shelter and overwintering areas, plant resources, or alternative hosts and prey [28,29,30]. Nevertheless, the existing variability in vegetation composition, habitat structure, or microclimate conditions across habitat types can differently shape local insect communities [11,31,32]. Plant architectural complexity is a key factor in structuring invertebrate assemblages in natural and semi-natural habitats [33,34] and habitat structure may be more important than plant species diversity for taxa with a variety of feeding modes such as Heteroptera [35]. Heteropterans represent an important component of the global insect fauna in agroecosystems and are potential indicators of overall biodiversity [36,37,38,39]. This group exhibits a significant morphological and ecological diversity, containing species with different functional traits including feeding type, specialization, or mobility [33,37,40,41,42]. They successfully use a wide range of habitats and are well-adapted to marked seasonal changes of environmental conditions [43]. All these attributes deeply determine organisms’ distribution, with changes in diversity levels often accompanied by changes in community trait composition [44].
When evaluating insect assemblages in human-disturbed habitats, the use of a taxonomic perspective coupled with a trait-based approach allows us to improve interpretation of how different habitat features or disturbances drive insect assemblages [32,45]. This is because, combined with species identity, functional traits provide information on biological and ecological characteristics that can condition organisms’ response to environmental factors. Therefore, evaluating changes in species and trait composition within a community could facilitate the identification of the main factors that constraint animal response, enhancing conservation efficiency.
Over the last decade, there has been a growing tendency to apply trait-based approaches when evaluating mechanisms underlying community structure or organisms’ interactions with biotic and abiotic factors [46,47]. Trait-based approaches—including morphology, feeding, life history, physiology, and behavior—measure the functional component of biodiversity, which influences ecosystem function performance and organism resilience, and allows us to reveal mechanisms behind community structures [47,48].
Functionally similar species can be similarly affected by environmental filters because the set of traits determine organisms’ responses to environmental conditions [49]. The distribution of insects is closely related to the availability of the resources they exploit; organisms exhibiting different feeding strategies may differ in their response to both environmental conditions and habitat features [42,50,51,52]. When more than one feeding strategy is considered, the trait-based approach is especially useful to understand the response of communities to environmental change [53]. However, it is noteworthy that not all traits are related to the same ecological features. For example, body size is related to attributes such as dispersal ability, sensitivity and response to habitat disturbance, as well as spatial niche or trophic, competitive, and facilitative relationships within ecological networks [44,54]. By contrast, body shape is associated with microhabitat use, while femur shape and wing length are related to dispersal ability and disturbance avoidance. Additionally—and particularly in heteropterans—rostrum length is associated with penetration depth [38,42], and thus with resource use. Changing environmental conditions or habitat characteristics can filter all these functional traits, thereby shaping all aspects of functional diversity or community composition [44,49,53]. Understanding community dynamics within non-cropped areas and identifying factors driving these dynamics is key to proposing conservation strategies that allow the enhancement of taxonomic and functional diversity, and thus the mitigation of biodiversity losses within agroecosystems.
In this study, we apply both taxonomic and trait-based approaches to assess heteropteran assemblages in Mediterranean vineyard agroecosystems. As a result of human influence as well as topographical and climatic variability, the Mediterranean Basin is characterized by dramatic spatial heterogeneity and strong seasonality [55], the latter imposing severe temporal differences in habitat properties and thus a high temporal heterogeneity. These changing conditions have an effect on shaping plant and insect communities [55,56,57]. With all these in mind, we assess, in Mediterranean vineyard agroecosystems, the role of non-cropped linear habitat type and seasonality in driving heteropteran assemblages on the basis of their species composition and addressing their morphometric trait composition. Within linear habitats, hedgerows exhibit a high structural complexity and a great temporal stability, providing a suitable diversity of resources over the season. On the contrary, grass strips are comparatively less structurally complex elements and more temporally changing habitats that offer transient resources. In heteropterans, taxonomic composition and morphometric traits are affected by habitat characteristics and environmental disturbances [39,44,49] and organisms exhibiting different feeding strategies may differ in their response to such characteristics [42,50,51,52]. Considering this, we set out to answer the following questions: (1) Do variations in habitat features, stability, and resource availability, derived from habitat type, determine the species composition of the heteropteran community? (2) How does the effect of seasonality on heteropteran assemblage differ among linear habitat types? (3) Are morphometric traits differently shaped by habitat type and seasonality among trophic guilds? We hypothesize that hedgerows, being more complex than grass strips, will support a greater richness and abundance of heteropterans and that community composition will vary between them. Additionally, we expect that differences in habitat features drive trait community composition, organisms with different feeding strategies differing in their response to environmental characteristics. Moreover, since different traits cover different functions and are proxies of varying levels of tolerance against disturbances, dispersal abilities, or microhabitat and food resource use, we predict heteropteran community traits in grass strips to differ from those of hedgerows and that those traits change over the season.

2. Materials and Methods

2.1. Study Area

The study was undertaken in 2014 across an area of 604 ha of traditional vineyard crops located in La Rioja, Northern Spain (42°27′ N, 2°38′ W) (Figure 1). The climate of the region is Mediterranean with continental influence. The average annual temperature varies from 12 to 13 °C and the mean annual precipitation is 400 mm. Vineyards are located on hillsides between 432 and 746 m a.s.l., with small- and medium-sized fields of overall less than 1 ha. Production is regulated by the Rioja Qualified Designation of Origin (Rioja DOCa) and is predominantly conventional. The soil within vineyards is artificially maintained as bare by ploughing and applying herbicides. Vegetative growth in vineyards reaches its maximum in July and early August, during which dense vine canopies can be found. Different types of ecological infrastructures are interspersed between vineyards, including mostly linear habitat elements such as hedgerows, as well as woodland patches (Figure 1 and Figure 2). Vegetation in non-cropped areas includes sclerophyllous woods and thicket formations composed of species such as Quercus ilex L., Quercus coccifera L., Rubus ulmifolius Schott, Rosa canina L., Dorycnium pentaphyllum Scop., Cistus albidus L., Lonicera etrusca Santi, Daphne gnidium L., Lavandula pedunculata (Mill.) Cav., and Thymus vulgaris L.

2.2. Sampling Design

Twelve linear habitat elements (mean length 140.6 ± 35.5 m), belonging to two different typologies, grass strips and hedgerows, were selected, maintaining the highest possible degree of uniformity in terms of shape and aspect (Figure 1 and Figure 2). These linear habitats were characterized by different plant species compositions and are structurally different (i.e., complexity and heterogeneity). Grass strips were dominated by grass and flowering herbaceous species, with few shrubs and fruit trees (low structural diversity), whereas hedgerows consisted of tree and shrub species, including R. ulmifolius, R. canina, and local plant species typically associated with Mediterranean forests, such as Q. coccifera or Q. ilex (high structural diversity).
Heteropterans were sampled monthly from May to September 2014 in the twelve linear habitats studied (six grass strips and six hedgerows). Each sampling was carried out during three consecutive days, randomly assigning the order in which the linear elements were sampled. The sampling period in each month was selected to ensure similar weather conditions within each of the five sampling periods. Given that sampling technique could have an influence on the species captured, and also in order to obtain an adequate representation of the community, we used a combination of two sampling methods: beating trays and pitfall traps. Canopy heteropterans were collected by beating trees and shrubs with a wooden stick while holding a beating tray (1 m in diameter) underneath to catch the falling specimens. In each linear habitat and on each month, five trees and/or shrubs of different species (when possible) were randomly selected and beaten for 2 min along different strata (low, medium, and high). In addition—and also for each linear habitat and month—twelve standardized pitfall traps were used to collect ground-dwelling insects. They consisted of plastic pots (9 cm in diameter) filled with 100 mL of a mixture of 70% alcohol and 10% antifreeze/coolant in a 3:2 ratio. The traps remained active in the field for three days. Collected heteropterans were transferred to 70% ethanol and then sorted into nymphs and adults and identified to species level.

2.3. Trait Definition and Measurement

According to their feeding mode, heteropterans were classified into phytophages, predators, and omnivores. For the adult individuals, six morphometric measurements were taken (body length and width, right forewing length, rostrum length, and right hind femur length and width), from which four morphometric traits were calculated [44]: body shape, hind femur shape, relative wing length, and relative rostrum length. Body shape is associated with microhabitat use and hind femur shape is a proxy of jumping ability; additionally, relative wing length is related to dispersal and disturbance avoidance, and relative rostrum length is an indicator of food resource use [44,49]. Body shape was calculated by dividing body length by body width, and hind femur shape by dividing the femur length by its width. Wing and rostrum lengths were defined as relative to body length. All measures were taken with a micrometer under a stereomicroscope.

2.4. Statistical Analysis

We applied generalized linear models (GLM) to analyze the effects of the linear habitat type (hedgerow and grass strip) and the seasonality (sampling month) on heteropteran species richness and abundance. Models were tested for independence by the auto-correlation function (ACF), finding no temporal correlation. A negative binomial error structure was used to control for overdispersion. Optimal models were selected by applying a likelihood ratio test (LRT). After that procedure, minimum models including only significant variables and interactions were obtained.
A permutational multivariate analysis of variance (PERMANOVA) was conducted to analyze spatial (hedgerow vs. grass strip) and temporal (over sampling months) changes in heteropteran community composition. The analysis was based on 9999 permutations. Among sampling months, pair-wise a posteriori comparisons were additionally made based on 9999 permutations.
Variations in body length, body shape, wing length, hind femur shape, and rostrum length within guilds across grass strips and hedgerows and temporal changes in those traits were estimated by fitting generalized linear models (GLM) with Gaussian distribution. Separated models were fitted for each morphometric trait. Specimen measurements were included as dependent variables and the linear habitat type, the month, the guild and their interactions as explanatory variables. All the models were tested for independence using the auto-correlation function (ACF). Temporal correlation was found only for body length, for which an autoregressive moving average (ARMA) model was fitted to the residuals of a generalized least squares (GLS) regression model (restricted maximum likelihood estimation) [58]. The ARMA structure for the model was defined by fitting models with different structures and comparing them using AICc. To meet the assumption of homoscedasticity, the family was included in the model as a variance covariate. All optimal models were obtained by using a likelihood ratio test (LRT). All the analyses were performed with R 4.0.3 software [59].

3. Results

We collected a total of 201 adult heteropterans from 55 different species that belonged to the families Alydidae (2), Anthocoridae (49), Coreidae (10), Cydnidae (4), Lygaeidae (77), Miridae (29), Nabidae (2), Pentatomidae (14), Pyrrhocoridae (2), Rhopalidae (3), and Tingidae (9). Among them, Beosus maritimus Scopoli, 1763 (Lygaeidae), and Orius laevigatus Fieber 1860 (Anthocoridae) were the dominant species. Regarding their diet, 90 specimens were phytophages, 58 predators, and 53 omnivores.

3.1. Taxonomical Response of the Community

Results from the GLMs showed that species richness was significantly affected only by the month; richness values increased in June compared to May and declined gradually over the rest of the season (Table 1, Figure 3a). Concerning abundance, there was a significant interactive effect between the type of linear habitat type and the month, with abundances over the months, varying differently in hedgerows compared to grass strips (Table 1, Figure 3b). In this sense, abundances in hedgerows increased in June compared to May and decreased progressively over the rest of the season, whereas grass strips showed a more heterogeneous pattern.
When analyzing spatio-temporal community structure, PERMANOVA revealed that variations in heteropteran assemblages between hedgerows and grass strips was only marginally significant (Table 2). In addition, pair-wise comparisons showed that heteropteran species composition did not change significantly over all the sampling months, and only May and June differed from the rest of the months in their composition (except for September) (Table 2).

3.2. Response of Morphometric Traits

When analyzing body length response, results showed that there is an interactive effect between the linear habitat type and the trophic guild. In this manner, omnivores’ mean body length was similar in hedgerows and grass strips, whereas it was greater in hedgerows in the case of phytophages and higher in grass strips in predators (Table 3, Figure 4a). Mean body length also varied over the season, increasing considerably from May to June, remaining relatively constant over the rest of the season.
Body shape marginally differed between linear habitat types in all guilds, the Heteroptera community being composed on average by thinner individuals in hedgerows, and by thicker specimens in grass strips (Table 3). Additionally, a significant effect of the month on body shape was observed, with a change from (on average) thicker specimens in May to thinner individuals in June, then remaining constant (Table 3).
Concerning hind femur shape, there was an interaction between the trophic guild and the linear habitat type, and also between guild and month (Table 3, Figure 4b,c). In omnivorous heteropterans, hind femur shape was similar in hedgerows and grass strips, whereas it differed between linear habitat types in phytophages and also in predators, those differences being more marked for the latest. The specimens of both guilds exhibited, on average, thinner femora in hedgerows compared to grass strips. Changes across the season also differed among guilds: femur shape remained roughly constant over the months in omnivorous and phytophagous heteropteran assemblages; in contrast, the predatory Heteroptera community changed progressively, from May to July, from specimens with on average thicker femora to individuals with thinner femora, thereafter remaining constant.
Upon analyzing the response of wing length relative to body length, we did not detect an effect of the habitat type and results only revealed a significant interaction between trophic guild and sampling month (Table 3, Figure 4d). Mean wing length of the omnivorous heteropteran assemblage decreased as the season progressed, whereas it slightly increased in both phytophages and predators.
Finally, concerning rostrum length relative to body length, interactive effects of the trophic guild and the linear habitat type, and also of the trophic guild and the sampling month, were detected (Table 3, Figure 4e,f). In omnivorous heteropterans, mean rostrum length did not differ between the specimens in hedgerows and those of grass strips. On the contrary, rostra were on average longer in hedgerows compared to grass strips in both phytophagous and predatory heteropteran assemblages. Rostrum response to seasonality also varied among trophic guilds. Mean rostrum length remained roughly stable over the months in the case of omnivorous and phytophagous heteropteran assemblages, while increasing progressively in May, June, and July in the case of predators, then remaining constant.

4. Discussion

Our findings provide strong evidences on how linear habitat type and seasonality drive heteropteran assemblages in Mediterranean vineyard agroecosystems, in terms of taxonomical and trait composition. Overall, habitat features shape morphometric traits of heteropteran communities, such traits additionally shifting over the season, although the responses varied across the different trophic guilds.

4.1. Taxonomical Response of the Community

In vineyard agroecosystems, linear habitats have been shown to support high levels of heteropteran diversity, community structure being largely determined by plant abundance and diversity or vegetation architecture [39,60,61,62]. Hedgerows are structurally diverse and botanically complex elements that potentially provide a wide range and a high amount of resources [51,63,64,65]. In addition, their plant composition, dominated by shrub-arboreal vegetation, makes these linear elements more stable over time than grass strips. By contrast, grass strips or weedy margins can occasionally offer diverse resources to this group of insects [39]. Having this in mind, we would expect that hedgerows support greater richness and abundance of heteropterans than grass strips. However, although hedgerows and grass strips differed in their species composition, habitat type was not as determinant in driving richness and abundance as seasonality. In fact, species richness was only affected by month, and abundance by the interaction between the month and the linear habitat type. Summer drought is a defining feature of the Mediterranean climate, with at least two consecutive months of dryness (July and August) occurring during the hottest period of the year; during this time, herbaceous plants dry out [66,67,68], thus leading to deep changes in habitat features. This drastic seasonality can affect temporal dynamics in insect communities and can lead to a peak of activity during late spring and early summer [57,69]. In addition to factors derived from climate conditions, local community composition is determined by multiple factors, including competition or food availability [70]. In accordance with this, we found that species richness was high early in the season (May to June) both in hedgerows and grass strips, then declining in the succeeding months probably as a consequence of changes in resource diversity. However, temporal variation in abundance was different in each linear element. Hedgerows adjusted to the expected tendency, while strips exhibited a very heterogeneous pattern over time. These different trends may be driven by differences in habitat stability, since the fact of being dominated by herbaceous plants that dry out in summer makes grass strips less stable structures that offer temporary resources such as pollen and prey.

4.2. Response of Morphometric Traits

Heteropterans are highly sensitive to particular habitat features, such as vegetation composition and structure, or resource availability, so these factors can drive their assembly patterns [71]. Accordingly, our results showed that trait composition of the heteropteran community was determined by both the linear habitat type and seasonality, with clear differences among trophic guilds.
Body size is a key trait related to several physiological, life-history, and ecological features. Within insects, body size would be associated to characteristics such as sensitivity and tolerance against disturbances, home range, spatiotemporal distribution, or dispersal ability, a dominant factor in shaping arthropod communities within agricultural systems [44,45,54,72,73,74]. Small size arthropods have less resource requirements and are comparatively more tolerant than large size arthropods, which associate with more stable habitats [74]. This pattern is consistent with our findings in phytophagous heteropterans, which were on average larger in hedgerows, more stable habitats than grass strips. Conversely, predators exhibited larger bodies in grass strips compared to hedgerows. This could reflect how grass strips are less stable microhabitats which offer more unpredictable resources and favor more mobile predators with a greater facility to access resources [75]. In addition, maneuverability of large predators through the habitat can be hampered in habitats with a more complex vegetation [76]. Predator response to changes in vegetation composition is in line with what might be expected since it has been shown that predatory heteropterans, and particularly generalist predators, are highly sensitive to vegetation diversity [77].
On the other hand, body shape is associated with microhabitat use, and habitat complexity may have an important influence on this trait [49,78]. Previous studies [44] found that grasslands, with greater proportions of grass species, are dominated by thinner heteropterans (i.e., higher body shape value; length/width). Accordingly, we would expect the heteropteran community in grass strips to be dominated by thinner specimens. However, we found the opposite: heteropterans were thinner in hedgerows. Topography in the area consists of traditional vineyards interspersed with non-cropped areas (i.e., woodland patches, hedgerows, grass strips), shaping a patchy agricultural landscape [73]. The majority of heteropterans are considerably mobile species with, in general, a high dispersal potential, hence they are able to access resources in the surrounding habitats [52,79]. Accessibility to different habitat types could facilitate heteropterans to obtain resources from the vicinity, therefore changing the way in which local habitat features determine the presence of heteropteran species with a specific body shape. Thus, other local habitat features, such as microclimate conditions, soil conditions, vegetation architecture, and pollution might affect heteropteran body shape distribution across the vegetation [37,60,77,80].
Community mean hind femur shape changed between linear habitat types and over the season differently in each tropic guild. Phytophagous and predatory heteropterans had on average thicker femora in grass strips compared to hedgerows. Thick hind femurs are related to greater jumping ability, which involves faster movements and higher mobility [40,44,81]. This condition may facilitate access to resources and thus may confer an advantage in grass strips, in which resource availability is less predictable. Accordingly, and given that the drastic seasonality of the Mediterranean climate implies a marked variation in resource availability over the months [66,67,68], we would expect to find a progressive change to thicker femora as the season progresses. Nevertheless, average femur shape remained broadly unchanged in omnivores and phytophages, and shifted to thinner femora in predators. Thus, other factors linked to seasonality more than resource availability may be conditioning the response of this trait. In the specific case of predators, communities were progressively dominated by Orius laevigatus (Fieber) (Anthocoridae), a common generalist predator in Mediterranean agroecosystems [82,83] which might be driving the observed pattern. However, caution is needed with regard to omnivores, as their decline in abundance throughout the season may impose a limitation on detecting a trend.
Wing length has been considered a proxy of dispersal ability and is also related to disturbance avoidance capacity [44,49]. Then, given the deep changes in habitat structure or resource availability in the Mediterranean region [66,67,68], it can be expected this morphometric trait to be sensitive to seasonality in a similar way in all trophic guilds. However, a different response was found among guilds. In phytophagous and predatory heteropterans, more limited than omnivores in encountering food resources [71,84], the slight shift toward longer wings as the season progresses might be driven by higher mobility and food resources accessibility in the surrounding habitats [52,85]. This is in contrast with omnivorous heteropterans, which use a wider range of resources and are more tolerant to habitat change and disturbance [62], and for which we would expect wing length to remain constant (similar to that occurring with other morphological traits), instead of showing lower mean values over the season. Nevertheless, again the low abundances could limit the identification of patterns in omnivores.
Rostrum length is known to be related to food resource use and varies across feeding types [49,78], and we found that both phytophages and predators, but not omnivores, were affected by linear habitat type, exhibiting on average shorter rostra in grass strips than in hedgerows. It has been shown that, in highly disturbed areas, heteropteran communities are dominated by specimens with on average shorter rostra [44]. The vegetation structure makes hedgerows to be more stable habitats than grass strips, which are more susceptible to undergoing disturbances derived from management [86].

5. Conclusions

Our results shed light on identifying what traits are selected against variations in habitat characteristics. We demonstrate that the trait-based perspective, including information of both morphometric traits and trophic guilds, is a sensitive and informative approach that allows not only to identify the factors that shape insect communities but also to propose the dynamics underlying these changes.
Variability in vegetation composition and structure or differences in resource availability among habitats and over the season are factors of major significance in driving species composition. However, we found that taxonomical response to changes in habitat characteristics was weaker than morphometric trait response, although trait response varied across trophic guilds because each of them exhibit particular requirements and are limited by specific factors. In this manner, the lower specialization regarding diet of omnivorous heteropterans makes community trait composition stay stable when compared to those traits of phytophagous and predatory heteropteran communities, more constrained by changing resources, and these shifted in response to the evaluated factors. Morphometric trait perspective highlights how habitats or environments with less stable conditions can lead to the selection of specific traits linked to high dispersal ability, which could mean a higher mobility across the agricultural matrix. Ultimately, different habitat types harbor a different trait composition. Grass strips support predators with on average larger bodies and thicker femora compared to hedgerows. This could lead to greater mobility and a wider range of prey, which in turn may impact prey suppression. On the contrary, hedgerows harbor larger phytophages with on average longer rostra, which is related to penetration depth and could thus lead to a broader range or resource use.
Since habitat features are major factors in structuring heteropteran communities, maintaining a variety of linear habitat types is essential to achieve a high local and landscape species richness and functional diversity [87]. High levels of diversity guarantee resilience, which is extremely relevant in changing environments, such as agricultural systems, that are subject to high levels of disturbance. On the other hand, maintaining a high diversity at multiple scales also enhance ecosystem functioning and the provision of key ecosystem services as conservation biological control [88,89], which is meaningful within the context of agricultural areas.
In addition, the role of the different linear habitats in driving heteropteran assemblages can experience regional variations, derived from changing environmental conditions, especially in areas with a marked seasonal variability such as the Mediterranean area. Within these changing environments, specific features of the different linear elements can buffer the effects of the dramatic changes linked to seasonality. This emphasizes the need to develop studies at different spatial scales that allow a better understanding of the significance of landscape elements on shaping insect assemblages across different climatic regions.
On the other hand, due to the significance of seasonality in driving insect trait-shifting across agricultural landscapes, temporal dynamics must be addressed when evaluating insect assemblage structure, especially in areas with highly changing environmental conditions such as those in the Mediterranean region. Finally, we encourage future research to assess partial uses and temporal dispersion dynamics among agricultural landscape elements for a broader understanding of their implications in shaping insect community traits, and to evaluate how functional community composition is related to ecosystem functions such as herbivory and predation.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su141912435/s1. Supplementary Materials File S1: Raw data.

Author Contributions

Conceptualization, N.R.-R., J.D.A. and L.B.-P.; methodology, N.R.-R., J.D.A. and L.B.-P.; software, N.R.-R., J.D.A. and L.B.-P.; validation, N.R.-R., J.D.A. and L.B.-P.; formal analysis, N.R.-R.; investigation, N.R.-R., J.D.A., M.G., I.B.-T. and L.B.-P.; resources, N.R.-R., J.D.A. and L.B.-P.; data curation, N.R.-R.; writing—original draft preparation, N.R.-R.; writing—review and editing, N.R.-R., J.D.A., M.G., I.B.-T. and L.B.-P.; visualization, N.R.-R.; supervision, J.D.A. and L.B.-P.; project administration, N.R.-R., J.D.A. and L.B.-P.; funding acquisition, N.R.-R., J.D.A. and L.B.-P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of Salamanca (Programa I: A2021-USAL).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available in the Supplementary Materials.

Acknowledgments

We are thankful to the Consejería de Agricultura, Ganadería y Medio Ambiente del Gobierno de La Rioja for providing the necessary permits to carry out the samplings. We also wish to thank Nadja Simons for her valuable and constructive revision on the first version of our manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Parameter estimates for the models assessing the effect of the evaluated factors on species richness and abundance, and on the different heteropteran morphometric traits.
Table
Table A1. Parameter estimates for the generalized linear models (GLM) assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), and their interaction on species richness and abundance of heteropterans. Only significant variables and interactions are shown. Reference coefficients are habitat (hedgerow) and month (May) (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001).
Table A1. Parameter estimates for the generalized linear models (GLM) assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), and their interaction on species richness and abundance of heteropterans. Only significant variables and interactions are shown. Reference coefficients are habitat (hedgerow) and month (May) (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001).
Response VariableIndependent Variabledfχ2p FactorEstimate ± SEzp
Species richness (GLM) (Intercept)−0.29 ± 0.34−0.840.3986
Month429.8135.343 × 10−6***Month (June)1.44 ± 0.383.750.0002***
Month (July)1.10 ± 0.402.760.0057**
Month (August)0.58 ± 0.431.340.1794
Month (September)−0.12 ± 0.50−0.240.8123
Abundance (GLM) (Intercept)0.92 ± 0.481.890.0587●
Habitat type17.3390.0067**Habitat (strip)−2.71 ± 1.18−2.290.0223*
Month46.1430.1887 Month (June)0.55 ± 0.660.830.4079
Month (July)0.38 ± 0.670.570.5675
Month (August)−0.41 ± 0.71−0.570.5677
Month (September)−1.10 ± 0.78−1.410.1573
Habitat × Month414.3520.0063**Habitat (strip): Month (June)3.28 ± 1.342.440.0145*
Habitat (strip): Month (July)2.51 ± 1.361.850.0646●
Habitat (strip): Month (August)4.04 ± 1.372.960.0031**
Habitat (strip): Month (September)4.09 ± 1.412.900.0037**
Table
Table A2. Parameter estimates for the models assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), the trophic guild (omnivore, phytophage and predator) and their interactions on the different heteropteran morphometric traits. Only significant variables and interactions are shown. Reference coefficients are habitat (hedgerow), month (May), and guild (omnivore) (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001; GLS: generalized least squares model; GLM: generalized linear model).
Table A2. Parameter estimates for the models assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), the trophic guild (omnivore, phytophage and predator) and their interactions on the different heteropteran morphometric traits. Only significant variables and interactions are shown. Reference coefficients are habitat (hedgerow), month (May), and guild (omnivore) (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001; GLS: generalized least squares model; GLM: generalized linear model).
Response VariableIndependent Variabledfχ2p FactorEstimate ± SEtp
Body length (GLS) (Intercept)6.18 ± 0.5211.950.0000***
Habitat type10.0500.8227 Habitat (strip)−0.10 ± 0.45−0.220.8229
Trophic guild2542.316<2 × 10−16***Guild (phytophage)−1.22 ± 0.36−3.380.0009***
Guild (predator)−5.04 ± 0.24−21.300.0000***
Month44.3610.3594 Month (June)0.87 ± 0.491.790.0748●
Month (July)0.89 ± 0.491.840.0680●
Month (August)0.75 ± 0.481.560.1213
Month (September)0.74 ± 0.481.540.1249
Habitat × Guild211.5850.0031**Habitat (strip): Guild (phytophage)−0.97 ± 0.60−1.630.1046
Habitat (strip): Guild (predator)1.13 ± 0.562.020.0450*
Body shape (GLM) (Intercept)2.94 ± 0.1519.20<2 × 10−16***
Habitat type13.3260.0682●Habitat (strip)−0.18 ± 0.10−1.820.0699●
Trophic guild241.7838.4× 10−10***Guild (phytophage)−0.71 ± 0.11−6.460.0000***
Guild (predator)−0.52 ± 0.14−3.800.0002***
Month423.88.7× 10−5***Month (June)0.75 ± 0.164.700.0000***
Month (July)0.46 ± 0.172.800.0057**
Month (August)0.61 ± 0.183.320.0011**
Month (September)0.50 ± 0.202.520.0126*
Hind femur shape (GLM) (Intercept)7.55 ± 0.7210.55<2 × 10−16***
Habitat type10.1760.6751 Habitat (strip)0.21 ± 0.500.420.6757
Trophic guild211.7920.0028**Guild (phytophage)0.15 ± 0.800.180.8540
Guild (predator)−2.17 ± 0.92−2.350.0199*
Month41.5480.8182 Month (June)0.08 ± 0.870.100.9228
Month (July)−0.47 ± 0.89−0.520.6015
Month (August)−0.17 ± 1.34−0.120.9019
Month (September)0.20 ± 1.240.160.8742
Habitat × Guild27.3030.0260*Habitat (strip): Guild (phytophage)−1.23 ± 0.55−2.210.0283*
Habitat (strip): Guild (predator)−1.88 ± 0.73−2.590.0104*
Guild × Month818.6070.0171*Guild (phytophage): Month (June)−1.50 ± 0.96−1.570.1193
Guild (predator): Month (June)1.23 ± 1.191.030.3045
Guild (phytophage): Month (July)0.04 ± 0.980.040.9684
Guild (predator): Month (July)1.70 ± 1.221.390.1680
Guild (phytophage): Month (August)−0.15 ± 1.42−0.110.9140
Guild (predator): Month (August)1.24 ± 1.560.800.4276
Guild (phytophage): Month (September)−1.27 ± 1.36−0.940.3510
Guild (predator): Month ( September)0.93 ± 1.480.630.5302
Wing length (GLM) (Intercept)0.92 ± 0.0422.23<2 × 10−16***
Habitat type11.2640.2609 Habitat (strip)−0.02 ± 0.02−1.120.2626
Trophic guild211.4630.0032**Guild (phytophage)−0.18 ± 0.06−3.220.0015**
Guild (predator)−0.17 ± 0.07−2.340.0205*
Month429.3196.74 × 10−6***Month (June)−0.26 ± 0.05−5.370.0000***
Month (July)−0.23 ± 0.06−3.930.0001***
Month (August)−0.27 ± 0.11−2.450.0154*
Month (September)−0.24 ± 0.11−2.180.0304*
Guild × Month817.7870.0229*Guild (phytophage): Month (June)0.19 ± 0.063.100.0023**
Guild (predator): Month (June)0.25 ± 0.092.740.0069**
Guild (phytophage): Month (July)0.25 ± 0.073.450.0007***
Guild (predator): Month (July)0.26 ± 0.092.840.0051**
Guild (phytophage): Month (August)0.26 ± 0.122.140.0340*
Guild (predator): Month (August)0.29 ± 0.132.260.0252*
Guild (phytophage): Month (September)0.25 ± 0.122.030.0439*
Guild (predator): Month ( September)0.31 ± 0.132.420.0167*
Rostrum length (GLM) (Intercept)0.37 ± 0.0216.76<2 × 10−16***
Habitat type10.1840.6678 Habitat (strip)0.01 ± 0.030.430.6683
Trophic guild217.0620.0002***Guild (phytophage)0.01 ± 0.030.260.7920
Guild (predator)−0.14 ± 0.04−3.600.0004***
Month40.4230.9805 Month (June)0.00 ± 0.03−0.130.8991
Month (July)0.00 ± 0.030.030.9735
Month (August)−0.01 ± 0.06−0.150.8820
Month (September)0.03 ± 0.060.560.5732
Habitat × Guild213.4130.0012**Habitat (strip): Guild (phytophage)−0.06 ± 0.03−2.140.0342*
Habitat (strip): Guild (predator)−0.14 ± 0.04−3.660.0003***
Guild × Month819.4860.0125*Guild (phytophage): Month (June)0.03 ± 0.040.830.4061
Guild (predator): Month (June)0.12 ± 0.062.130.0343*
Guild (phytophage): Month (July)0.01 ± 0.040.150.8848
Guild (predator): Month (July)0.17 ± 0.053.160.0019**
Guild (phytophage): Month (August)0.05 ± 0.070.700.4847
Guild (predator): Month (August)0.141.840.0677●
Guild (phytophage): Month (September)−0.03−0.480.6332
Guild (predator): Month ( September)0.13 ± 0.071.790.0750●

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Figure 1. Location of the study area in La Rioja, Northern Spain; location of the twelve linear habitats (hedgerows and grass strips) sampled across the study area (obtained from Google Earth, 2020).
Figure 1. Location of the study area in La Rioja, Northern Spain; location of the twelve linear habitats (hedgerows and grass strips) sampled across the study area (obtained from Google Earth, 2020).
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Figure 2. Two linear habitat types were studied: hedgerows (a) and grass strips (b). Both linear elements are interspersed between vineyards across the landscape (c).
Figure 2. Two linear habitat types were studied: hedgerows (a) and grass strips (b). Both linear elements are interspersed between vineyards across the landscape (c).
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Figure 3. Estimated mean ± SE of (a) species richness in each month, and (b) abundance in hedgerows (black dots) and grass strips (green dots) in each month. Dull dots represent raw data.
Figure 3. Estimated mean ± SE of (a) species richness in each month, and (b) abundance in hedgerows (black dots) and grass strips (green dots) in each month. Dull dots represent raw data.
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Figure 4. Estimated mean ± SE of (a) body length in hedgerows and grass strips for each trophic guild; (b) hind femur shape in hedgerows and grass strips for each trophic guild; (c) hind femur shape in each month for the different trophic guilds; (d) wing length (relative to body size) in each month for the different trophic guilds; (e) rostrum length (relative to body size) in hedgerows and grass strips for each trophic guild; (f) rostrum length (relative to body size) in each month for the different trophic guilds. Dull dots represent raw data.
Figure 4. Estimated mean ± SE of (a) body length in hedgerows and grass strips for each trophic guild; (b) hind femur shape in hedgerows and grass strips for each trophic guild; (c) hind femur shape in each month for the different trophic guilds; (d) wing length (relative to body size) in each month for the different trophic guilds; (e) rostrum length (relative to body size) in hedgerows and grass strips for each trophic guild; (f) rostrum length (relative to body size) in each month for the different trophic guilds. Dull dots represent raw data.
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Table
Table 1. Results of the generalized linear models (GLM) assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), and their interaction on species richness and abundance of heteropterans (** p < 0.01, *** p < 0.001). Parameter estimates for the models are provided in Appendix A, Table A1.
Table 1. Results of the generalized linear models (GLM) assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), and their interaction on species richness and abundance of heteropterans (** p < 0.01, *** p < 0.001). Parameter estimates for the models are provided in Appendix A, Table A1.
Response VariableIndependent Variabled. f.χ2p
Species richness (GLM)Month429.8135.343 × 10−6***
Abundance (GLM)Habitat type17.3390.0067**
Month46.1430.1887
Habitat × Month414.3520.0063**
Table
Table 2. Results of the PERMANOVA analyses for heteropteran assemblage, testing spatial (linear habitat type: hedgerow, grass strip) and temporal variability (sampling month) on species composition. Pair-wise comparisons between sampling months (May, June, July, August, and September) are also provided (● p < 0.1, * p < 0.05, ** p < 0.01).
Table 2. Results of the PERMANOVA analyses for heteropteran assemblage, testing spatial (linear habitat type: hedgerow, grass strip) and temporal variability (sampling month) on species composition. Pair-wise comparisons between sampling months (May, June, July, August, and September) are also provided (● p < 0.1, * p < 0.05, ** p < 0.01).
Species Composition
Global modelPairwise comparisons
Variabled. f.MSR2Fp MonthFp
Habitat type10.62610.03361.39820.068●May vs. June 2.06930.004**
Month40.58550.12561.30740.023*May vs. July 1.47500.078●
Residuals350.44780.8408 May vs. August1.40680.089●
Total40 1.0000 May vs. September1.18090.367
June vs. July 1.40920.067●
August vs. June1.58950.037*
August vs. July0.98060.497
September vs. June1.09590.33
September vs. July0.89730.658
September vs. August0.82020.737
Table
Table 3. Results of the models assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), the trophic guild (omnivore, phytophage, and predator) and their interactions on the different heteropteran morphometric traits (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001; GLS: generalized least squares model; GLM: generalized linear model). Parameter estimates for the models are provided in Appendix A, Table A2.
Table 3. Results of the models assessing the effect of the linear habitat type (hedgerow, grass strip), the temporality (sampling month), the trophic guild (omnivore, phytophage, and predator) and their interactions on the different heteropteran morphometric traits (● p < 0.1, * p < 0.05, ** p < 0.01, *** p < 0.001; GLS: generalized least squares model; GLM: generalized linear model). Parameter estimates for the models are provided in Appendix A, Table A2.
Response VariableIndependent Variabled. f.χ2p
Body length (GLS)Habitat type10.0500.8227
Trophic guild2542.316<2 × 10−16***
Month44.3610.3594
Habitat × Guild211.5850.0031**
Body shape (GLM)Habitat type13.3260.0682●
Trophic guild241.7838.4 × 10−10***
Month423.88.7 × 10−5***
Hind femur shape (GLM)Habitat type10.1760.6751
Trophic guild211.7920.0028**
Month41.5480.8182
Habitat × Guild27.3030.0260*
Guild × Month818.6070.0171*
Wing length (GLM)Habitat type11.2640.2609
Trophic guild211.4630.0032**
Month429.3196.74 × 10−6***
Guild × Month817.7870.0229*
Rostrum length (GLM)Habitat type10.1840.6678
Trophic guild217.0620.0002***
Month40.4230.9805
Habitat × Guild213.4130.0012**
Guild × Month819.4860.0125*
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Rosas-Ramos, N.; Asís, J.D.; Goula, M.; Ballester-Torres, I.; Baños-Picón, L. Linear Landscape Elements and Heteropteran Assemblages within Mediterranean Vineyard Agroecosystems. Sustainability 2022, 14, 12435. https://doi.org/10.3390/su141912435

AMA Style

Rosas-Ramos N, Asís JD, Goula M, Ballester-Torres I, Baños-Picón L. Linear Landscape Elements and Heteropteran Assemblages within Mediterranean Vineyard Agroecosystems. Sustainability. 2022; 14(19):12435. https://doi.org/10.3390/su141912435

Chicago/Turabian Style

Rosas-Ramos, Natalia, Josep D. Asís, Marta Goula, Iván Ballester-Torres, and Laura Baños-Picón. 2022. "Linear Landscape Elements and Heteropteran Assemblages within Mediterranean Vineyard Agroecosystems" Sustainability 14, no. 19: 12435. https://doi.org/10.3390/su141912435

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