Introduction
There is a tendency of species to retain the ancestral niche of their
lineage, i.e. niche conservatism, and different niches may hence be
occupied by different lineages (Crisp & Cook 2012). Niche conservatism
is the necessary condition for related species to coexist locally
(Prinzing et al . 2016, 2017). However, if environmental
conditions change rapidly and organisms are sessile and long lived then
niche conservatism may produce local neighbourhoods that are distantly
related, such as a tree immigrating into a zone that recently became
abiotically suitable but is still occupied by distant relatives. This
and other processes result in phylogenetic isolation between a focal
organism and its neighbours (Cavender-Bares et al . 2009).
Coexistence with distant relatives may change species interactions to
the advantage or the disadvantage of the focal individual (Webb et
al . 2002; Yguel et al . 2011; Verdú et al . 2012; Gerholdet al . 2015; Prinzing et al . 2017). However, it remains
unknown what are the consequences of coexistence with distant relatives
for the plant’s contribution to ecosystem functioning, such as the
recycling of its own carbon (C) and nitrogen (N) through decomposition.
For sessile, big, long lived organisms like trees that grow and
germinate in their own litter such an ecosystem feedback would be
essential for maintenance and reproduction - and thereby the capacity of
species to track conserved niches under rapid environmental change
(Ackerly 2003).
Plant litter decomposition is an important and complex ecosystem
function depending on multiple abiotic (e.g. temperature and
moisture conditions), biotic factors (i.e. plants and soil
organisms) and their interactions (Coûteaux et al . 1995;
García-Palacios et al . 2013; Santonja et al . 2015). This
process is governed, firstly, by the quantity and quality (i.e.physico-chemical characteristics) of litter that was produced by plants,
providing microhabitats and food resources for soil organisms. These
soil organisms are then the main actors of the decomposition process
controlled by i) the abundance and diversity of soil organisms (Fig. 1a,
Trajectory T1, Cornwell & Weedon 2014) and ii) the efficiency by which
these soil organisms decompose a given litter (Fig. 1a, Trajectory T2).
Even though the process is largely driven by soil organisms, a part of
the decomposition process is abiotically driven resulting from leaching
losses of mineral ions and small organic molecules (Fig. 1a, Trajectory
T3). These different trajectories will leave different statistical
signatures (Table 1). Below, we will hypothesize how phylogenetic
isolation of a focal tree might operate on each of these trajectories.
We hypothesize that phylogenetic isolation of a focal tree from its
neighbors influences the decomposition of the tree’s litter due to
aboveground mechanisms, i.e. mechanisms changing litter quality (Fig.
1b). Specifically, phylogenetic isolation aboveground (PIA) strongly
reduces phytophagy of the focal tree (Yguel et al . 2011) and
phytophagy is closely linked to the leaf litter quality (Schädleret al . 2003). For example, phytophagy can induce the production
of secondary metabolites such as phenolics
(Schultz
& Baldwin 1982;
Karban
& Myers 1989; Coley & Barone 1996; Strauss & Agrawal 1999). These
compounds negatively affect abundance and efficiency of decomposer
organisms but also the abiotic decomposition of litter (Trajectories T1
and T2 in hypothesis PIA1, and PIA2 in Table 1). On the other hand,
phytophagy can increase the leaf damage and in turn increase the
accessibility of leaf litter for soil decomposers (PIA3, Cárdenas &
Dangles 2012), as well as for moisture and desiccation (PIA4, Ritchieet al . 1998). Finally, phylogenetic isolation from neighbours may
also impose a stress on the focal trees due to unfavorable competitive
or microclimatic conditions (e.g. lower soil pH or moisture
conditions). Such stress may trigger increased investment into, again,
phenolics and/or carbon-rich compounds (Fernandez et al . 2016),
impacting decomposers numbers and efficiency as well as abiotic
decomposition of litter (PIA5 and PIA6).
We also hypothesize that phylogenetic isolation of a focal tree from its
neighbors influences decomposition of the tree’s litter due to
belowground mechanisms (Fig. 1b). On the one hand, a phylogenetically
distant neighborhood produces a litter that is dominated by distantly
related plant lineages and may select for soil biota particularly
capable of decomposing this dominant litter (Ayres et al . 2009;
Austin et al . 2014; Pan et al . 2015; Cheng & Yu 2020),
but naïve for decomposing the litter of the focal tree. Decomposition of
the focal tree’s litter might hence suffer from a phylogenetic
away-field disadvantage (PIB1 in Table 1), a so far untested phenomenon
equivalent to taxonomic away-field disadvantage that has been often
demonstrated (Gholz et al . 2000; Negrete-Yankelevich et
al . 2008; Vivanco & Austin 2008). On the other hand, mixing of litter
from distantly related focal and neighbor trees may trigger
complementarity effects: transfer of nutrients among litters might
increase decomposer abundance, diversity and activity and hence
decomposition (PIB2, Lummer et al . 2012; Handa et al .
2014; Porre et al . 2020). Transfer of toxins among litters, in
contrast, might decrease decomposers and their efficiency and hence
decomposition (PIB3, Hättenschwiler & Vitousek 2000; Gessner et
al . 2010). Finally, some neighboring lineages may degrade the physical
environment in which the focal tree decomposes, e.g . by
decreasing soil pH (PIB4) and soil moisture conditions (PIB5) or by
increasing thermal fluctuations due to delayed budburst (PIB7, Yguelet al . 2014) and thereby a shorter vegetation period (PIB8).
Other neighboring lineages might improve the physical environment in
which the focal tree decomposes, e.g. by decreasing soil soaking
and hence increasing aeration (PIB6, Cornelissen et al . 2017;
Dias et al . 2017). Overall, phylogenetic isolation of a focal
tree affects the pool of decomposers, their resources and the physical
background, but consequences for decomposition remain unknown.
As decomposition below a given tree will be the result of a mixture of
both aboveground and belowground processes, we designed a litter bag
experiment for trees growing among phylogenetically closely or distantly
related neighbors, i.e. under low or high phylogenetic isolation
(PI, Fig. 1c). To our knowledge, this is the first ‘phylogenetic
litter-transplantation’ experiment. Such an approach exposes litter from
both high-PI and low-PI trees under a given tree to identify effects of
PI operating via aboveground processes. Moreover, the approach
exposes litter from a given tree under both high-PI and low-PI trees to
identify the effects of PI operating via belowground processes.
We studied oaks (Quercus petraea ), a system for which effects of
phylogenetic isolation on enemy pressure and budburst have been
demonstrated already (e.g. Yguel et al . 2011; Yguelet al . 2014) and for which major shifts in ranges of suitable
climate are predicted (Hansen et al . 2001; Iverson & Prasad
2001; Barton 2002).
To identify ecosystem consequences of coexistence with distantly related
neighbours we tested a set of increasingly complex predictions from
hypotheses in Table 1: (1) Phylogenetic isolation above (PIA) and/or
belowground (PIB) per se changes the rate at which litter decomposes (in
terms of mass loss, C-loss and N-loss). (2) PIA and/or PIB changes the
trajectories by which litter decomposes: the abundances and diversities
of different soil biota controlling decomposition, the efficiency by
which a given group of soil biota at a given abundance decompose litter,
the putatively abiotic effects that are not attributable to soil
organisms considered (Fig. 1a). As soil biota we accounted for the
dominant groups Acari, Collembola and microorganisms, and, for a
subsample, for fungi. Moreover, trajectories invoking higher decomposer
activities should lead to a strong relative accumulation of13C (Bowling et al . 2008) and we hence tested
whether PIA and/or PIB changes the13C/12C signatures. (3) The effects
of PIA or PIB can be replaced, and hence likely explained by, litter
traits and/or environmental characteristics as outlined above and in
Table 1.