Age and level of self-organization affect the small-scale distribution of springtails (Collembola) 1, 2 1 3 LINA A. WIDENFALK , HANS PETTER LEINAAS, JAN BENGTSSON, AND TONE BIRKEMOE
1Department of Ecology, Swedish University of Agricultural Sciences, P.O. Box 7044, Uppsala, SE-75007 Sweden 2Department of Biosciences, University of Oslo, P.O. Box 1066, Blindern, Oslo, N-0316 Norway 3Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, As, NO 1432 Norway
Citation: Widenfalk, L. A., H. P. Leinaas, J. Bengtsson, and T. Birkemoe. 2018. Age and level of self-organization affect the small-scale distribution of springtails (Collembola). Ecosphere 9(1):e02058. 10.1002/ecs2.2058
Abstract. In studies of community assembly, species are often assumed to have similar spatial distribu- tions and responses to the environment regardless of age or size. Under this assumption, it is possible to use species and species-level traits in community composition studies. Here, we test this assumption for two species of soil-living arthropods (springtails: Collembola) with direct development but assumed differ- ences in self-organizing behavior. We expected that the species with more pronounced social interactions (Hypogastrura tullbergi) should be less influenced by environmental factors and species interactions across all age classes, than Folsomia quadrioculata that is not known to exhibit social behavior. We used variance partitioning to examine the relative contributions of soil variables, vegetation composition, and other Collembola, vs. spatial variables (as a proxy for intraspecific interactions, i.e., self-organization), on the distribution of the two species and three of their age classes. We show that two coexisting species with clear aggregation patterns greatly differ in how much the environment contributes to affecting the species’ spatial structure. Local F. quadrioculata abundance was explained by different spatial and environmental variables depending on age class. In contrast, for H. tullbergi, spatial variables explained more of the abundance variation in all age classes. These differences have implications for the general predictability of changes in spatial structuring of species, as self-organized species may be less likely to respond to changes in environmental factors. Our results show that because age classes may be differentially affected by environmental conditions, caution should be taken when assuming that species traits can be applied to all developmental stages in a species.
Key words: age classes; biological interaction; Collembola; environmental constrain; intraspecific interaction; Moran’s eigenvector map analysis; population ecology; self-organization; soil fauna; spatial configuration; variance partitioning.
Received 2 October 2017; revised 20 November 2017; accepted 22 November 2017. Corresponding Editor: Uffe N. Nielsen. Copyright: © 2018 Widenfalk 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. E-mail: [email protected]
INTRODUCTION (Lima et al. 2009). To develop theories of com- munity organization, we need to describe pat- Relating the spatial structure of species and terns that can be compared across systems, and populations to environmental conditions is a first this needs to be done at all the scales that could step to understanding the factors underlying spe- influence the system (Levin 1992). Analyses of cies distributions and community composition spatial community distribution patterns com- (Cottenie 2005). This is important for manage- monly view all conspecifics as behaving similarly ment of both threatened species and pest species and as having the same traits (McGill et al. 2006)
❖ www.esajournals.org 1 January 2018 ❖ Volume 9(1) ❖ Article e02058 WIDENFALK ET AL. a practice that has been criticized by Violle et al. performing spatial analyses (Tilman and Kareiva (2012). Rudolf and Rasmussen (2013) added to 1997, Borcard et al. 2004, Griffith and Peres-Neto this criticism by emphasizing the risk of missing 2006, Beale et al. 2010). One of the most promis- important differences between life stages (i.e., ing to capture spatial patterns at a range of scales age classes) when traits are used at the species simultaneously are Moran’s eigenvector map level. This risk seems especially high in species (MEM) analyses (Borcard et al. 2004, 2011). Spa- where food or habitat requirements are dramati- tial variables can be interpreted as representing cally different between juveniles and adults, as in either dispersal constrains or biotic interactions many amphibians and most insects. However, causing distinct spatial distribution patterns not species that live in the same macro-habitat connected to environmental variables (Cottenie throughout their lives might also differ in their 2005). Fine-scale spatial patterns are more likely spatial distribution with age: For example, in to be connected to biotic interactions. These connection with reproduction, feeding prefer- fine-scalepatternsarepossibletocaptureby ences, drought or temperature tolerance, and MEM analyses, whereas larger scale descriptors strength of interspecific interactions may show such as trend surface analyses usually fail age-specific differences (Gilbert et al. 1999, (Borcard et al. 2004). Amarasekare and Sifuentes 2012). The Collembola (springtails) are excellent Most populations show spatial structuring study organisms to test whether the species level within their habitat (Tilman and Kareiva 1997). is a reliable unit for spatial distribution analyses. However, the degree of spatial structuring and its Their lower dispersal ability compared to, for causes vary greatly among species. Both biotic example, flying insects makes their immediate and abiotic factors, including environmental con- presence at a site much less stochastic. And with ditions, interactions with other species and direct development, with juveniles and repro- resources, may cause individuals to aggregate in ducing adult stages usually co-occurring in the specific areas (Wiens 1976). Species may also same habitat (Hopkin 1997), age dependency show “self-organized” spatial structuring (sensu will be more subtle and general, than the extreme Parrish and Edelstein-Keshet 1999), that is, a differences in organisms with metamorphosis behavior not driven by specific habitat or envi- and switching of resources between juveniles ronmental factors, but caused by internal factors and adults. However, in some Collembola spe- within a population, such as responses on odor cies, age classes show different preferences (pheromones), vocal or visual stimuli. Reasons regarding food quality (Jensen et al. 2006). This for aggregation, not directly related to environ- indicates that there may be age-related differ- mental variables, include reducing the risk for ences in behavior that can result in different predation (Hamilton 1971), increasing reproduc- distribution patterns even in this taxon, which tive success (Levitan and Young 1995), or can have effect on, for example, the function of improved ability to detect favorable patches (Lei- the species in the ecosystem (Sato and Watanabe naas et al. 2015), as well as other benefits of social 2014). In addition, dispersal might be more group living (Benoit et al. 2009, Vanthournout restricted in young individuals (Johnson and et al. 2016). The degree to which self-organized Wellington 1983), both as a function of smaller behavior influences the spatial distribution of size, but also due to a restricted ability to use all individuals depends on its relative dominance micro habitats because of a higher sensitivity to over sensitivity to environmental factors. In addi- drought (Leinaas and Fjellberg 1985, Hertzberg tion to these current conditions, present distribu- and Leinaas 1998). Since eggs are deposited in tion patterns may to varying degree also reflect batches, and often by aggregating adults past structuring processes owing to dispersal lim- (Hopkin 1997), reduced dispersal of smaller itation. Effects of these drivers on spatial distribu- stages may lead to age differences in aggregating tion will in many organisms be age dependent, tendency even without self-organization of the and comparison of juveniles vs. adults may juveniles. As collembolans have an important reveal important components of the dynamics. ecosystem functioning through their role in Space can be described in several different decomposition and nutrient cycling of soils ways, and there are a number of methods for (Petersen 1994), and different species and life
❖ www.esajournals.org 2 January 2018 ❖ Volume 9(1) ❖ Article e02058 WIDENFALK ET AL. stages may have different level of impact, it is (Hertzberg et al. 1994), while its drought sensi- important to understand underlying mecha- tivity may further affect its spatial distribution nisms for their spatial distribution to be able to (Hertzberg and Leinaas 1998). However, no dis- predict potential changes in functioning (Wardle tinct group coordination has been observed in 2006). this or any related species in the field, nor during The tendency to aggregate is diverse and extensive lab studies of the species (Sengupta widespread among collembolan taxa (Hopkin 2015). We therefore hypothesize that environ- 1997 and references therein), ranging from spe- mental constrains will be more important than cies where environmental variation explains self-organized aggregation in this species. In most of the local-scale distribution patterns contrast, H. tullbergi belongs to a genus where (Hertzberg et al. 1994, Chauvat et al. 2014), to advanced coordinated group behavior is com- species with advanced coordinated group behav- mon (Lyford 1975, Simon 1975, Mertens and ior (Lyford 1975, Leinaas 1981). This species- Bourgoignie 1977, Leinaas 1983, Leinaas et al. specific difference in self-organizing behavior 2015). Although less striking in H. tullbergi than makes studies on species distribution patterns many other species of the genus, we nevertheless particularly interesting. Attraction by chemical hypothesized that the spatial structuring of this communication has been shown repeatedly in species would have a more distinct self-orga- many Collembola since the first documentations nized component than F. quadrioculata. We also in the 1970s (Mertens and Bourgoignie 1977, Ver- expected the two species to differ in how age hoef and Nagelkerke 1977, Verhoef et al. 1977). classes vary in their responses to environmental In many species, aggregation pheromones have factors. Age-dependent effects of environmental been studied by the tendency to aggregate in stressors such as drought is hypothesized to be experimental arenas when exposed to substances more pronounced in the sensitive F. quadrioculata excreted or extracted from conspecifics (Verhoef (Hertzberg and Leinaas 1998). In contrast, all age and Nagelkerke 1977, Verhoef et al. 1977, Benoit stages appear much more robust in H. tullbergi, et al. 2009). Under field conditions however, as even the smallest animals are seen active such effects may not necessarily be sufficiently together with larger ones even in fairly dry habi- strong to clearly influence the spatial structuring tats (H. P. Leinaas, personal observation). Hence, of populations. The distribution of individuals we hypothesized that potential difference in may then be mainly explained by variation in sensitivity between age classes in this species will environmental conditions, such as resources and not have consequences for spatial structuring humidity (Hertzberg et al. 1994, Chauvat et al. between the age classes, as it is expected to be 2014). On the other hand, there are also species counteracted by the predicted self-organized with advanced group behavior based on volatile aggregation. pheromones keeping the members of the group Both species were studied within an area of together even when moving around (Mertens ~6m2 in a homogeneous dry meadow in the and Bourgoignie 1977, Leinaas 1983). high Arctic ecosystem on Svalbard; in this In this study, we investigate the relative impor- particular habitat, they are among the most tance of environmental factors vs. self-organized dominant species of Collembola (Fjellberg 1994). intraspecific behavior for the small-scale spatial We disentangled the relative effect of environ- distribution of species and age classes within two mental constrains (soil properties, vegetation, collembolan species, Hypogastrura tullbergi and other Collembola) from that of spatial fac- (Schaffer)€ and Folsomia quadrioculata (Tullberg). tors (self-organization, or dispersal limitations) Both species show clear tendencies to aggregate by variance partitioning of the explained spatial in high Arctic tundra meadows (Hertzberg et al. variation in abundance of each species or age 1994, Sømme and Birkemoe 1999). Based on class. Additionally, we discuss the ecological available information, we predicted that the relevance of the specific explanatory variables underlying mechanisms for the spatial aggrega- explaining the distribution of each species and tion would differ between the two species. In age class and the potential consequences of patchy habitats, F. quadrioculata may be seen to using species-level data in analyses if age classes aggregate where food conditions are favorable show different spatial structuring.
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