Early Successional Colonizers Both Facilitate and Inhibit the Late Successional Colonizers in Communities of Dung-Inhabiting Insects

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Early Successional Colonizers Both Facilitate and Inhibit the Late Successional Colonizers in Communities of Dung-Inhabiting Insects EUROPEAN JOURNAL OF ENTOMOLOGYENTOMOLOGY ISSN (online): 1802-8829 Eur. J. Entomol. 118: 240–249, 2021 http://www.eje.cz doi: 10.14411/eje.2021.025 ORIGINAL ARTICLE Early successional colonizers both facilitate and inhibit the late successional colonizers in communities of dung-inhabiting insects FRANTISEK X.J. SLADECEK 1, 2 , SIMON T. SEGAR 1, 3 and MARTIN KONVICKA1, 2 1 University of South Bohemia in Ceske Budejovice, Faculty of Science, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic; e-mails: [email protected], [email protected], [email protected] 2 Biology Centre, Czech Academy of Sciences, Institute of Entomology, Branisovska 31, 370 05 Ceske Budejovice, Czech Republic 3 Agriculture & Environment Department, Harper Adams University, Newport, Shropshire, TF10 8NB, UK Key words. Diptera, Coleoptera, dung-inhabiting insects, competition, heterotrophic succession, successional mechanisms Abstract. The infl uence of early arriving species on the establishment and activity of later ones (the priority effect) is a key issue in ecological succession. Priority effects have been extensively studied in communities subject to autotrophic succession (plants, sessile animals), but only sporadically studied in communities subject to heterotrophic succession (e.g. dung or carrion inhabiting communities). We studied the infl uence of early successional colonizers on late successional colonizers by manipulating the suc- cessional processes in cow dung pats via delaying, and thus lowering, colonization by early successional insects. The decreased activity of early successional insects did not affect the species richness of late successional insects, but it did lead to increased abundance of colonizers. Late successional coprophagous beetles were facilitated by early successional species while larvae of late successional coprophagous fl ies were inhibited, presumably, by the larvae of early successional fl ies. We therefore propose that both facilitation and inhibition have a role to play in the heterotrophic succession of coprophilous insects. In addition, facilita- tion and inhibition among taxa seems to refl ect their evolutionary relationships, with facilitation being prominent between phylo- genetically distant lineages (early successional Diptera and late successional Coleoptera), and inhibition being more common between closely related lineages (early vs. late successional Diptera). These patterns are strikingly reminiscent of the situation in the autotrophic succession of plants. INTRODUCTION Wootton (1993) refi ned these ideas and added two more Succession is one of the most studied phenomena in scenarios describing the partial effect of early successional community ecology, yet the mechanisms behind the pat- species; i.e., that the early successional species can support terns observed are still not completely known. Succession- or hinder the establishment of the late successional spe- al processes either lead to the establishment of a more or cies. This stands in contrast to a strict dichotomy between less stable community (autotrophic succession, e.g., for- enabling and disabling establishment under the facilitation mation of forests on lava islands), or to the disintegration and inhibition models). of the resource and loss of all species from the commu- Successional mechanisms have traditionally (Clements, nity (heterotrophic succession, e.g. dung decomposition) 1916; Gleason, 1926, 1927) and primarily been studied (Begon et al., 2006). in the context of autotrophic plant communities and ses- How early colonizers infl uence the species richness and sile animals, which have been long supposed to follow the abundance of later ones (priority effects) is a major fi eld of inhibition or tolerance models (Connell & Slatyer, 1977). study in successional theory. Priority effects typically lead However, in all such communities, it is more typical to see to one of three outcomes and are driven by distinct pro- a combination of several models during the course of suc- cesses (Connell & Slatyer, 1977). The facilitation model cession, so that facilitation and inhibition often co-occur predicts that early successional species enable the estab- (Callaway & Walker, 1997; van der Putten, 2009; Walker lishment of the late successional ones; the inhibition model et al., 2010; Maggi et al., 2011). For example, a nurse plant predicts that early successional species prevent the estab- only facilitates seedlings within a limited distance (Dickie lishment of late successional ones; and the tolerance model et al., 2005), or facilitation applies only under high levels predicts late successional species to establish themselves of environmental stress (Vazquez et al., 1998). The level irrespective of the activity of the early successional ones. of facilitation also depends on the patristic evolutionary Final formatted article © Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice. An Open Access article distributed under the Creative Commons (CC-BY) license (http://creativecommons.org/licenses/by/4.0/). 240 Sladecek et al., Eur. J. Entomol. 118: 240–249, 2021 doi: 10.14411/eje.2021.025 distances between plant species. Evolutionarily distant such as dung degradation (DeCastro-Arrazola et al., 2020). lineages tend to facilitate each other while closely related Dung insect communities are also threatened by land use lineages tend to compete (Verdú et al., 2009; Castillo et changes (Buse et al., 2015) and the overuse of veterinary al., 2010). products with non-target effects (Tonelli et al., 2020). In contrast, there are still only a limited number of studies These threats mean that understanding dung community targeting the mechanisms behind heterotrophic succession, dynamics is of relevance to maintaining ecosystem ser- which was originally supposed to follow the facilitation vices in conservation efforts (Cimon-Morin et al., 2013). model (Connell & Slatyer, 1977). The reality is, how- Specifi cally, we address the following questions: ever, inevitably more complex with both facilitation and (1) Does delaying insect access, and therefore limit- inhibition at work. Dung insect communities have shaped ing access of early successional species, enable/disable much of this thinking. For example, early successional (models sensu Connell) or improve/hamper (models sensu dung beetles can facilitate the activity of late successional Wootton) the activity of late successional dung-inhabiting earthworms which hasten dung degradation (Holter, 1977, insects? 1979). On the other hand, late successional dung beetles (2) Is there a preference of late successional groups of tend to be outcompeted by early successional ones to such insects towards dung with previously high (controls) or a point that late beetles are more abundant in moths when low (treatment) activity of early successional species? early beetles are scarce (Davis, 1989). Moreover, early suc- cessional beetles are supposed to facilitate the invasion of MATERIAL AND METHODS late successional beetle predators and fl ies (Hammer, 1941; Study site Mohr, 1943). In large carcasses, early successional larvae The study was carried out on a 23 ha pasture, situated 10 of blowfl ies (Calliphoridae) were reported to facilitate car- km west of Ceske Budejovice, Czech Republic (48°59´2.4˝N, rion degradation following the bloated stage (Pechal et al., 14°24´34.957˝E), Central Europe. This pasture hosts a permanent 2014), and thus facilitate the invasion of late succession- herd of 30 adult cows and has been continuously grazed for dec- al beetles (Sharanowski et al., 2008). On the other hand, ades. It is situated at 380 m a. s. l., in a region with a mean annual elimination of some dominant early successional blowfl y temperature of 8.1°C, mean annual precipitation of 620 mm, and a vegetation season spanning from March to October (Sladecek species increased the diversity of late successional fl ies et al., 2013). from other families (Pechal et al., 2014). Furthermore, a high abundance of early successional blowfl y is negatively Insect sampling correlated with the abundance of both early and late bee- Three sampling campaigns, covering the three main periods of tle and fl y species (Kadlec et al., 2019). This cumulative coprophilous insect activity, were carried out in 2011: spring (18 evidence, however, stems from individual studies. To date, April – 3 May); early summer (12–27 July) and early autumn (22 there has been no experimental focusing on interactions August – 6 September). We used artifi cially created cow dung pats of 1.5 l volume between early and late colonizers of ephemeral resource (approx. 25 cm in diameter) to mimic naturally deposited pats. patches. Finally, it is not yet clear which process exactly Fresh, recently defecated, un-colonized dung was obtained from a determines the correlational trends seen between early barn with permanently stalled cows. These cows were not treated successional and late successional species. This contrasts with any veterinary drug that could affect insect colonization and with studies of plant communities, where the level of fa- establishment (Rodríguez-Vívas et al., 2020). No insects were cilitation depends on the patristic evolutionary distances found to colonize the dung in the barn, since fresh dung is cleared between species (Verdú et al., 2009; Castillo et al., 2010). each day. We protected such dung from insect colonization before Here, we present a study focusing on mechanisms that exposition. At the study site, we thoroughly
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