Individual Spatial Niche Specialization Affects Species Interactions

Individual Spatial Niche Specialization

Introduction

Individuals of the same species do not occupy identical ecological niches.
Individual niche specialization extends the concept of ecological niche partitioning to the within-species level.
Interactions of individuals with the environment affect ecological interactions like competition and predator-prey relationships.
Behavior mediates these interactions; interindividual differences in behavior (animal personality) determine individual niche specialization.
Partitioning of space and time is a means of ecological niche differentiation.
Home range size, utilization patterns, and microhabitat distribution vary with personality.
Interindividual variation in behavior contributes to ecological niche specialization.
Non-random distribution leads to biased interactions towards certain behavioral types.
The effect of individual behavioral differences is more explored within species interactions, less so between species.
Behavioral-type composition changes interactions; aggressive to docile shifts interactions from amensalism to commensalism or mutualism.
The strength of mutualism scaled positively with shyness of fish individuals: Anemonefish (Amphiprion percula) and sea anemones (Entacmaea quadricolor).
Few studies consider individual differences in both interacting species.
Active predatory old field jumping spiders (Phidippus clarus) consumed inactive house crickets (Acheta domesticus) more often than active crickets and vice versa.
Mutualism between magpies (Pica pica) and rocky mountain elk (Cervus canadensis) is influenced by boldness in both species.

Competition

One of the most important interspecific interactions is competition over resources.
Competition determines species coexistence, community composition, and biodiversity.
Within-species variation in behavioral types affects a species' competitive ability.
These effects have rarely been demonstrated; indirect competition example: bolder sticklebacks (Gasterosteus aculeatus and Pungitius pungitius) consumed more prey.
Most studies on behavior and interspecific interactions are short-term lab experiments.
Spatial patterns in natural communities might provide insights into indirect interactions.
Empirical evidence for individual niches in co-occurring species and reciprocal effects on species interaction patterns is scarce.
Individual trophic niches in thin toed frogs (Leptodactylus spp.) are temporally and spatially flexible, and connected to community composition and dynamics.
Individual niche variation might influence species coexistence and regional biodiversity patterns.
Assessing spatial patterns of individuals of different species might provide insights into how individual niche specialization affects ecological interactions.
Movement and space use determine temporal and spatial aspects of resource competition.
Movement and space use are the outcomes of behavioral decisions, modified by boldness and exploration.
The effect of within-species variation in behavioral traits on between-species spatial interactions remains unknown.
Inferring patterns and strengths of spatial interactions requires information on space use of all potential interaction partners.
Small, ground-dwelling rodents allows to overcome this challenge because ecologically similar species co-occur in high densities, their spatial interactions are on an easily trackable scale and they inhabit areas with vegetation cover that can be quantified as a proxy for predation risk.
The study investigates spatial interaction patterns of bank vole (Myodes glareolus) and striped field mouse (Apodemus agrarius) to test if space use affects intra- and interspecific interactions.
Both species co-occur in central and eastern Europe, have similar habitat choices/diets, partially overlapping activity, suggesting resource competition.
Previous research showed space-use patterns in bank voles facilitated individual spatial niches, boldness was key, exploration marginal.
The main focus is whether behavioral-dependent individual spatial niche occupation covaries with spatial interactions with con- and heterospecifics.
The study measured interindividual differences in behavior within species and quantified spatial interactions within and between species.
The hypothesis is that individual differences in behavior are functionally integrated with intra- and interspecific spatial interactions.

Predictions

Boldness positively covaries with overlap of home ranges/core areas of heterospecifics due to the relationship between boldness and home range size.
For conspecifics, boldness negatively covaries with overlap due to higher spatial exclusivity on the intraspecific scale.
Bolder individuals spatially interact more with heterospecifics and less with conspecifics.
Boldness positively covaries with the number of neighbors (intra- and interspecific) within home ranges/core areas.
Boldness positively covaries with distances between the home range center of a focus individual and those of neighboring individuals (con- or heterospecific).
Exploration is not expected to covary with spatial interactions.

Material and methods

Study sites

Data was collected on five study sites within the AgroScapeLabs in northwestern Brandenburg, Germany (53°21′56.20″N, 13°48′17.30″E).
Region is characterized by intensive agriculture on large fields with small, island-like fallow lands and hedges.
Fallow lands served as study sites (size: 0.85 to 1.66 ha), heterogeneous vegetation of grasses, streaked with nettles (Poaceae 40%, Urtica spp. 21%, Ballota spp. 9%), bushes and trees.
Confined habitat islands are an ideal setting to investigate patterns and mechanisms of competition at a local scale.
Study sites were visited consecutively and on each study site, experimental procedures—capture–mark–recapture (CMR), individual differ- ence testing, VHF telemetry (see details below)—were done within a continuous time period of 13 ± 3 days.

Capture-mark-recapture

Between August and November 2016, CMR was conducted with Ugglan live traps.
At each study site, traps were set up in a grid consisting of 55 traps with ca. 10 m distance between them, grid shape depended on the shape of the habitat remnant.
Traps were baited before trapping for 24h with rolled oats and apples.
Upon initial capture, individuals were temporarily marked with a unique fur cut.
Individuals used for repeated behavioural testing were permanently marked with a passive integrated transponder (Euro ID, Trovan ID100) after their first test.
Trapping continued on each site until greater than 95% of the captured animals were marked.
Between 75 and 103 rodents were captured on each of the five study sites, representing a density of 84 to 234 rodents ha^{-1}, with bank vole and striped field mouse being the two most abundant species (51–81% of the captured individuals; 108–179 individuals ha^{-1}).
Other species included common vole (Microtus arvalis), field vole (M. agrestis), yellow-necked mouse (Apodemus flavicollis) and wood mouse (A. sylvaticus; species are presented with declining abundances).

Individual difference test

To quantify interindividual differences in behavior in both species, adult individuals (greater than 17 g) were subjected to an individual difference test directly after capture.
Tests were performed at the capture site at comparable locations on each study site.
The test set-up unites a dark–light test with an open-field test within one mobile set-up.
Test details are described in Schirmer et al. [36].
Briefly, in the dark–light test, individuals moved from the trap into an opaque plastic pipe (10.5 × 32 cm) with a swing door at each end, attached to a round arena (diameter 1.30 m, 30 cm height).
Within 300 s, latency to stick the head out of the pipe (latency head) and the latency to leave the pipe with the whole body (latency body) were quantified.
If an individual did not leave the pipe during the test, the latency was set to 300 s.
Once the individual entered the round arena, the open-field part of the test started.
In the open-field test, behavior is assessed based on the assumption that the middle of the arena (open, exposed; risky) and the border area (covered, not exposed; safe) represent different levels of perceived predation risk.
In this test part, the latency to enter the centre of the arena, the number of crossings, the number of sections entered, and the activity were quantified.
All variables were quantified via direct observations in the field by one observer (A.S.).
Tests were performed only on rainless days with low wind speed.
Tests were repeated for recaptured individuals (n = 57) 1–7 days later.

Automated radio telemetry

To assess movement and space use on a finer spatio-temporal scale, individuals at three study sites were equipped with VHF radio telemetry transmitters (1.1 g, BD-2C, Holohil Systems, Canada) on a collar, and tracked them for four days.
At each site and for each radio-tracked individual, tracking commenced 4.6 ± 3.5 days after the last individual difference test was per- formed.
Individuals were selected based on their recapture probability (greater than two captures before collaring) and body mass (greater than 20 g, i.e. transmitter weight less than or equal to 5% of body mass).
Females in the last stages of gestation, based on visual inspection were excluded.
In total, 21 bank voles (9 females, 12 males) and 15 striped field mice (6 females, 9 males) were radio-tracked.
All individuals on a respective site were tracked simultaneously during four consecutive days.
The automated VHF tracking system consisted of eight omnidir- ectional antennas placed around the trapping grid connected to two automated receiving units (ARU).
ARUs logged the signal strengths the antennas received from transmitters carried by animals.
Two-dimensional location points were calculated of radio-collared individuals based on two perpendicular isolines of distributions of signal strengths, creating an x- and y-dimension following the border lines of the site, respectively.
Isolines were calibrated with transmitters at known locations within each grid prior to data collection (for more details, see [36]).
On average 96 location points were sampled per day for each individual with an average location accuracy of 9.4 ± 7.3 m varying with vegetation density and air moisture.

Spatial analyses

Based on CMR data, for each individual tested for be- havioural differences a proxy was calculated for its centre of spatial activity as the arithmetic mean trapping point (mean ± s.d.: 4.3 ± 3.9 captures per individual; n = 227).
As a measure of the strength of the interaction between spatially interacting individuals, distances between each individual and its nearest neighbor (con- and heterospecific) were calculated.
Spatial analyses were con- ducted in the program QGIS (version 2.18.14).
Statistical analyses of these spatial interactions were restricted to adult individuals of known behavioural type because it is assumed that only these residential individuals (n = 126) have temporary stable home ranges within study sites; juveniles and transient individuals (captured only once) were excluded.
Given the resolution of tracking data, static spatial interactions patterns were assessed by calculating intra- and inter- specific home range overlaps for 95% and 50% kernel density estimations, representing the home ranges and core areas, with the package adehabitat (version 1.8.18 [37]) in the program R (version 3.3.0 [38]).
For each individual, these spatial overlap metrics were obtained by calculating its home range overlap with every other sim- ultaneously tracked individual at the study site.
Repeated sampling of individuals was corrected for in statistical models.
Additionally, QGIS was used to combined detailed data of spatio-temporal space use of radio-tracked individuals (n = 36) with intensive CMR data of the vast majority of individuals pre- sent at each study site and counted the number of conspecific and heterospecific neighbours that had their mean trapping point in the home range and the core area of each radio-tracked individual.

Statistical analyses

Individual differences

Repeatability was estimated for each behavioural variable observed during the individual difference test (§2c) using the R package rptR (version 0.6.405).
Repeatable behavioural variables were entered into a principal component analysis (PCA) with oblimin rotation to combine correlated variables into meaningful components; species was used as a categorical grouping factor.
PCA rendered two meaningful components, interpreted as exploration and boldness.
Individual scores on the components were used as repeated measures for exploration and boldness in the subsequent analyses; boldness was the focus.

Individual differences and interspecific spatial interactions

Bivariate Bayesian mixed-effects models, run with the package MCMCglmm, was used to assess covariance between boldness and spatial interaction parameters.
Covariances were interpreted significant if the credibility intervals did not include zero.
Bivariate Bayesian mixed-effects models were used with boldness and the intra- or interspecific overlap (home range or core area) as response variables; overlap metrices were calculated for each radio-tracked dyad of individuals per study site (intraspecific dyads: n = 202, interspecific dyads: n = 216).
Bivariate Bayesian mixed-effects models was used with boldness and the number of mean trapping points of con- or heterospecifics in a radio-tracked indi- vidual’s (n = 36) home range or core area as response variables.
Bivariate Bayesian mixed-effects model with boldness and the distance to the next con- or heterospecific as the response variables was applied.
The larger sample size (n = 126 individuals) allowed to include species, sex as well as the difference in boldness scores between individuals and whether individuals were of the same sex or of different sexes as fixed factors to assess a potential bias of spatial interactions.
All models were also run with exploration instead of boldness as a response variable in bivariate models.

Results

Interindividual differences in behavior

Almost all variables observed in the individual difference test were repeatable.
Species had no effect in the PCA.
Two meaningful com- ponents were extracted, which cumulatively explained 83% of the variance in the data.
The first component, representing exploration, explained 56% of the variance, and was comprised of the variables from the open-field test part (eigenvalue 3.15, all loadings greater than 0.7) and was repeatable over time (R = 0.17, 95% CIs = [0.04, 0.37], p = 0.04).
The second com- ponent, representing two latencies measured in the dark–light test part (eigenvalue 1.51, all loadings greater than 0.7), explained 27% of the variance and was interpreted as boldness.
This com- ponent was repeatable over time (R = 0.39, 95% CIs = [0.15, 0.59], p = 0.001).
Both components did not correlate at the phenotypic level (\rho = -0.09, p = 0.346).

General spatial interaction patterns

It was previously demonstrated that boldness scales positively with home range (mean ± s.d.: 2125 ± 1812 m^2) and core area (mean ± s.d.: 530 ± 472 m^2) sizes, as well as microhabitat characteristics of home ranges in bank voles
This pattern also pertains in striped field mice (home range size mean ± s.d.: 2737 ± 2046 m^2, core area size mean ± s.d.: 600 ± 446 m^2).

Intraspecific spatial interaction patterns

Intraspecific overlap of home ranges and core areas (n = 202 dyads based on tracking data) did not covary with individual boldness
The number of conspecific neighbors negatively covaried with the boldness of the focal individual on the home range scale.
Bolder individuals had fewer conspecific neighbors in their home range compared with shy individuals (based on tracking data, n = 36).
A positive covariance was obtained between boldness and the distance to the nearest conspecific (trapping data, n = 126).
Bolder individuals had larger distances to the nearest conspecific compared with shy individuals.
Species and sex had no effect.

Interspecific spatial interaction patterns

The bolder an individual, the higher its home range overlap with individuals of the other species (based on tracked individuals, n = 216 dyads), the larger the number of hetero- specific neighbors in its home range, and the lower the distance of its mean trapping point to that of its nearest heterospecific neighbor.
None of the fixed effects predicted variation in inter- specific interaction variables.
At the core area scale, neither the inter- specific overlap nor the number of heterospecific neighbors covaried with boldness.

Discussion

Consistent individual differences in boldness covary with space use of two rodent species.
Spatial interaction patterns between individuals were not random.
Behavioral types mainly differed in the relative importance of intra- versus interspecific competition.
Within-species variation along this competition gradient could contribute to maintaining individual niche specialization and facilitate species coexistence.

Personality-dependent spatial interactions within species

Individuals did not interact randomly in space with conspecifics.
Bolder individuals appeared to maintain high spatial exclusivity at the within-species level, indicated by lower numbers of conspecific neighbors in their home range and larger distances to nearest neighbors.
Under indirect competition, the strength of spatial interactions serves as a proxy for the intensity of resource competition.
Bolder individuals are probably facing reduced intraspecific compe- tition compared with shy individuals.
Boldness scales positively with home range and core area size and covaries with microhabitat characteristics associated with predation risk on the home range scale.
Consistent individual differences in bold- ness facilitated the occupation of individual spatial niches, which resulted in reduced interactions with conspecifics.
Behavioral-type-dependent niche differentiation should reduce intraspecific competition by decreasing the similarity of conspecifics, facilitating the maintenance of different behavioral types in natural populations.
Bolder individuals occupy microhabitats of better quality and/or have higher access to resources (e.g. food, shelter, predator- free area).

Personality-dependent spatial interactions between species

Spatial interactions between species were not random but varied with behavioral type.
Bolder individuals shared their home ranges with more heterospecific neighbors compared with shy individuals.
Spatial interactions among heterospecifics could indicate the strength of competition between them.
Boldness varied positively with interspecific overlap of home ranges and number of heterospecific neighbors in an individual’s home range.
The bolder an individual, the shorter its distance to the centre of activity of its nearest heterospecific neighbor.
Reduced intraspecific competition in bolder individuals appears to come at the cost of increased interspecific competition.
This behavioral-type- dependent pattern of intra- and interspecific competition could equalize potential competitive advantages between both types within species and facilitate their maintenance in the natural population.
The areas of the core areas might be kept exclusive independent of behavioral type.

Can spatial niche specialization facilitate species coexistence?

The hypothesis of within-species spatial niche specialization is supported.
Individuals depending on their behavioral type, occupy spatial niches varying in the relative importance of intra- versus inter- specific resource competition.
Given their high intraspecific competitive ability, bolder individuals can maintain large areas with more exclu- sive resource access.
Particularly bold individuals of the other species might move into these areas of reduced resource competition, ultimately creating non-random distribution patterns of behavioural types and biased patterns of intra- versus interspecific resource competition.
Different behavioral types choose different microhabitats and interaction environments (i.e. niche choice), or the environment drives the emergence of different behavioural types and associated interaction patterns (i.e. niche confor- mity).
Heterospecific interactions are biased towards individuals of one, similar behavioral type.
Resource competition might be increased for more similar behavioral types but decreased for less similar ones due to differential spatial interactions.
Consistent individual differences in behavior could be a largely overlooked aspect of limiting similarity because it contrib- utes to lowering the strength of competition between phenotypically different individuals.

Conclusion

In two ecological generalist and widely distributed rodent species, interindividual differences in behavior within species also pertain to interactions between species.
Boldness varied with space-use patterns of individuals, affecting spatial interactions between individuals, and ultimately led to the occupation of individual spatial niches.
Based on those niche differences, the competitive environment varies between individuals.
Individual spatial niche specializ- ation might facilitate the coexistence of species by restricting the interspecific interactions to a set of individuals from a population whose competitive strengths are balanced and by reducing the limiting similarity between individuals to a degree that allows stable coexistence.
Interindividual differences in behavior might mediate fine-scale niche parti- tioning between equivalent functional types within a trophic guild, possibly increasing local biodiversity.