Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L

Víctor González-García; Pedro J Garrote; Jose M Fedriani

doi:10.1371/journal.pone.0273311

. 2022 Aug 23;17(8):e0273311. doi: 10.1371/journal.pone.0273311

Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L.

Víctor González-García ^1,^*,^#, Pedro J Garrote ^2,^#, Jose M Fedriani ^3,^4,^*,^#

Editor: Ignasi Torre⁵

PMCID: PMC9398033 PMID: 35998189

Abstract

Although farmlands are the most extensive terrestrial biomes, the abandonment of traditional agriculture in many parts of the world has brought opportunities and challenges for the restoration of such human-disturbed habitats. Seed arrival is a crucial necessary ecological process during plant recolonization that can be enhanced by the use of the so-called “perch plants”. Little is known, however, about whether the seed arrival via frugivorous birds is affected by the spatial distribution of the perch plants in disturbed habitats. To evaluate several spatial aspects of “perching” effect, we used a spatially explicit approach in two disturbed plots within the Doñana National Park (SW Spain). Specifically, we chose as study system the pioneer Mediterranean dwarf palm Chamaerops humilis L., which is often used as a perch by a variety of frugivorous bird species. A total of 289 C. humilis individuals were sampled in search of bird feces (N = 2998) and dispersed seeds (N = 529). Recorded seeds belonged to six different woody species from five different families. Nine bird species from six different families were recorded using C. humilis as perches. GLMs analyses indicated that taller C. humilis males with higher numbers of spatially associated woody species received more dispersed seeds. We detected a random spatial structure of bird feces and dispersed seeds in one study plot, while a nonrandom spatial structure was found in the other one, where isolated C. humilis received a higher number of bird feces and dispersed seeds than expected under spatial null models. The difference in spatial patterns between both study plots could relate, among other factors, to their different state of development in the ecological succession. Most of dispersed seeds were concentrated in a small number of C. humilis individuals, usually male and large ones, that acted as “hotspots” of seed arrival. The fact that frugivorous birds in one study site visited most often isolated C. humilis questions the aggregated spatial structure of revegetation designs typically used in restoration projects. This study reveals novel spatial aspects of the “perching” effect which could be helpful in the restoration of human-disturbed habitats worldwide.

Introduction

Croplands and grazing lands have become the largest terrestrial biomes, occupying almost the 40% of Earth’s land surface [1, 2]. However, in the Mediterranean Europe, areas destined to agriculture have been reduced by 34.2% in the last half century. In Spain, specifically, they have decreased by 54.8% [3, 4]. This abandonment of farmlands represents an opportunity and a challenge to boost biodiversity through natural (and facilitated) revegetation and reforestation [5], and thus to restore habitats to the stages prior to human disturbances. Restoration projects are generally expensive given that they have been usually focused on planting dominant tree species [6]. Although many of such restoration projects have been successfully [7], they could be unaffordable when the affected area is too large, limiting the full recovery of vegetation structure [8]. Natural regeneration acts more widely and is less expensive than tree plantations [5], although its intensity varies by region and habitat. In arid and semiarid areas with low primary productivity such as the Mediterranean basin, natural regeneration is clearly slower [7, 9] than in more humid and productive environments like tropics or temperate regions, since the water availability for plants is an evident limitation [10]. Some other constrains in human-disturbed habitat restoration are inter- and intraspecific competition from herbaceous plants [11], the border effect or the past landscape pattern [12], and the limited propagule pressure and dispersal capacity of seeds [9, 13, 14].

Seed dispersal plays a key role in habitat dynamics and structure of plant communities [15]. Seed dispersal facilitates plant colonization of vacant areas and thus, the recovery of vacant human-altered habitats [16]. Birds and mammals are the main seed dispersers of most fleshy-fruited plants [17]. Many frugivorous birds often use tree and shrub branches as “perches”, i.e. sites where they defecate and regurgitate large number of viable seeds [18–20]. Repeated visits to the same perches locally increase seed arrival and thus can trigger nucleation processes [20]. Human-disturbed habitats are more prone to these nucleation effects, since they are often vacant habitats where perches are scarce, which promotes a marked seed clumping [21, 22]. However, we are not aware of any study that has quantified the patterns of seed clumping under perches using a spatially explicit approach.

Interestingly, in some cases, the same shrub species acting as perches also act as nurse plants, i.e. facilitating the emergence, growth and survival of other plant species, [23] which are designated as “beneficiary species”, promoting the natural (re)colonization [24, 25]. Chamaerops humilis L., is a pioneer Mediterranean palm crucial in habitat recovery [26]. Our unpublished data indicate that these palms potentially act as perches for many frugivorous birds, which play important roles as seed dispersers and agents of the natural recolonization of human-disturbed areas by woody plants (e.g. [27]). The facilitative role of this keystone palm has been recently evaluated [28]. In particular, [4] the dwarf palm has been found positively associated with multiple woody plant species in disturbed vacant habitats. By contrast, the “perching” effect of C. humilis and its potential implications for the ecological restoration of human-disturbed landscapes remain unknown. In addition, very little is known about the pervasiveness of the natural “perching” effect and its spatial aspects and scales. On this matter, Spatial Point Pattern Analysis (SPPA) constitutes a powerful tool to evaluate this sort of questions [29].

In this study we evaluate spatial patterns on the role of C. humilis as perch for frugivorous birds dispersing woody plant seeds in human-disturbed habitats. To achieve our goal, we selected two study plots within Doñana National Park (SW Spain) that differ in their history of human-driven perturbations and vegetation. We used a spatially explicit approach to answer the following questions: (i) How pervasive is the “perching” effect in our two studied human-disturbed habitats? (ii) Are there differences between the two study plots in the role of C. humilis as perch? And, if so, what are the factors underlying such differences? (iii) Do aggregated C. humilis receive more bird feces containing dispersed seeds? (iv) Do particular C. humilis individuals act as "hot spots" of seed arrival, and if so, why? And (v) Do the species of dispersed seeds correspond to the woody beneficiary species found spatially associated with the C. humilis?

Material and methods

Study species

Chamaerops humilis L. (Arecaceae), commonly known as “European fan palm” or “Mediterranean dwarf palm”, is an evergreen shrub endemic to the western Mediterranean [30, 31]. This palm can grow up to 10m tall, although individuals are not usually taller than 2m [32]. Leaves are big, fan-shaped and displayed in numerous segments, exhibiting several long thorns on the petiole. It is dioecious, with fruits only growing on female plants. Flowering occurs in spring, from March to May. Spread takes place through seeds (sexually) or, less commonly, through division of adult trees (asexually) [30]. Seeds are mostly dispersed by medium-sized carnivores such as Eurasian badgers Meles meles and red foxes Vulpes vulpes [33] but also by ungulates (e.g. red deer Cervus elaphus and wild boar Sus scrofa) some of which occasionally disperse seeds by regurgitation [34, 35].

The facilitative role of C. humilis and its capacity of recolonizing disturbed habitats have made it widely used in ecological restorations [36], although its role as nurse plant has only recently been demonstrated [4]. Chamaerops humilis protects seeds and seedlings of woody species from high temperatures and drought, as well as from herbivory thanks to the spikes present in its leaves [4, 37]. Frequent visits of some seed dispersers such as red foxes to fruiting C. humilis could increase perceived predation risk for several species of rodents (e.g. Apodemus sylvaticus) and lagomorphs (e.g. Oryctolagus cuniculus) [35] and thus locally lessen small mammal seed and seedling predation of beneficiary plants.

In its typical habitat, the Mediterranean scrubland, C. humilis is often spatially associated with Asparagus L. spp., Daphne gnidium L., Olea europaea L. var. sylvestris (Mill.) Hegi, Pistacia lentiscus L., Pyrus bourgaeana Decne, and other woody species. These spatial associations are thought to be due to a combination of “nursing” and “perching” effects [4, 30], although the “perching” effect has not been tested yet.

Study area and plots

The study was carried out within the Doñana National Park (SW Spain, on the west of the Guadalquivir River estuary). All permits necessary were granted by the National Park Service (ref. 2019/10) and the Junta de Andalucía (ref. 2019107300002261/IRM/MDCG/mes). The National Park presents a Mediterranean sub-humid climate, with most of rainfalls taking place from November to April, showing an average annual rainfall of 500-600mm [33], with hot dry summers (June-September) and mild humid winters (October-January).

We selected one early- and one late-successional study plots 10 km apart (Fig 1). Study areas are different in terms of vegetation, successional stage and human-use history [4, 38]. The early-successional plot (Matasgordas; 13.9 ha) has been historically and intensively affected by anthropic management of the vegetation and livestock pressure [39]. The eastern portion of this study plot was drastically modified in 1970 when most of woody plants (both shrubs and trees) were removed in order to create a “dehesa”, becoming an open area for cattle grazing with scattered trees, mostly Quercus suber L. and O. europaea var. sylvestris [4, 16]. In 1996, the land became owned by Government and happened to be under the protection of the National Park boundaries, putting an end to the cattle grazing. Once livestock was removed from the area, native fleshy-fruited plants such as C. humilis, D. gnidum, P. lentiscus and P. bourgaeana started to recolonize their habitat via seed dispersal by birds and mammals [4, 16]. Due to such past human activity, the area is now formed, mainly, by two habitats: (i) Scrubland dominated by P. lentiscus shrubs with some Q. suber and O. europaea var. sylvestris trees [4, 33] and (ii) an old-field, where our study plot was set, which woody vegetation is mainly composed by animal-dispersed native plants such as C. humilis, P. lentiscus, D. gnidium and P. bourgaeana, Asparagus aphyllus L., Halimium halimifolium (L.) Willk and Cistus salviifolius L. and scattered Q. suber and O. europaea var. sylvestris trees [4]. The distribution of C. humilis in this plot is very aggregated, and best described by a double-clustered component process with a random component process (with 22% of isolated C. humilis individuals; see S1 File and S1 Table).

Doñana Biological Reserve is located in the centre of the National Park. It is laid on a coastal plain distinguished for its flatness and being separated from the sea by lagoons and mobile dune systems. However, it is this closeness to the sea which allows a humid and mild climate [40] and enables the existence of three different types of habitats: marshland, dunes and scrubland; being the ecotone between the scrubland and the marshes (locally known as “La Vera”) where we set our late-successional study plot. This area has been historically managed by human for agriculture, hunting, cattle grazing and tree felling, especially O. europaea var. sylvestris and Q. suber [41]. Reserva was protected earlier than Matasgordas, in 1964 and it has been recovering ever since, being recolonised by animal-dispersed plants such as A. aphyllus, C. humilis, Phillyrea angustifolia L. or R. ulmifolius [4]. This scrubland is dominated by H. halimifolium and Stauracanthus genistoides (Brot.) Samp. with scattered trees of Q. suber, O. europaea var. sylvestris and Pinus pinea [33]. Our later-successional study plot presents higher density of shrubs than the one at the early successional study plot. Such a difference in shrub cover led to a greater abundance of fleshy fruits in the early-successional study plot, which likely makes this site more attractive to frugivorous birds [4]. The distribution of C. humilis in this plot was also best described by a double-clustered component process with a random component process (with 9% of isolated individuals; see S1 File and S1 Table).

Data collection

Every target C. humilis (109 and 180 in the early and late successional study plots, respectively) was individually georeferenced with a submetric GPS Leica 1200. Mean separation distances were 219 and 223 m in the early and late successional study plots, respectively. The density of C. humilis plants in the late-successional plot (7.8 individuals / ha) was pretty similar to the late-successional plot (8.41 individuals / ha). Each study plot was visited eight and five times along the seed dispersal seasons (i.e. from September to November) of 2019 and 2020, respectively. To control for potential temporal variations on bird abundance and seed dispersal along the dispersal seasons, both study plots were sampled during the same sampling days. Rainy days were avoided because of the low bird activity and the feces wash out on C. humilis.

During the sampling, which lasted about 3 h per day in the early-successional plot and about 2 h in the late-successional plot, any observed bird perching on focal C. humilis individuals was recorded. Overall, nine bird species were recorded perching: Cisticola juncidis, Lanius senator, Phoenicurus ochruros, Phylloscopus collybita, Pica pica, Saxicola rubicola, Sturnus unicolor, Sylvia atricapilla and Sylvia melanocephala (Fig 2, Table 1).

Fig 2 — (A) Eurasian magpie (*Pica pica*). (B) Common stonechat (*Saxicola rubicola*). (Photo credit: Pedro J. Garrote).

Table 1. Summary of collected data.

	EARLY-SUCCESSIONAL PLOT		LATE-SUCCESSIONAL PLOT
	2019	2020	2019	2020
Chamaerops humilis (individuals)	109		180
Number of feces	705	206	1560	527
Number of seeds	28	16	340	145
C. humilis with feces (%)	42.2	37.6	43.9	27.8
Feces with seeds (%)	3.3	17.8	7.5	7.8
C. humilis with seeds (%)	8.3	11.9	13.9	7.8
Asparagus aphyllus (seeds)	1	7	16	3
Daphne gnidium (seeds)	7	5	1	2
Olea europaea var. sylvestris (seeds)	0	0	26	8
Phillyrea angustifolia (seeds)	0	0	4	0
Pistacia lentiscus (seeds)	20	4	2	0
Rubus ulmifolius (seeds)	0	0	291	132
Perching birds
Cisticola juncidis	1	1	0	2
Lanius senator	0	0	2	0
Phoenicurus ochruros	0	0	3	1
Phylloscopus collybita	0	0	1	0
Pica pica	0	0	2	0
Saxicola rubicola	2	1	7	4
Sturnus unicolor	0	0	2	0
Sylvia atricapilla	1	1	1	2
Sylvia melanocephala	3	3	14	4
Beneficiary species
Asparagus aphyllus	35		96
Cistus sakviifolius	16		0
Daphne gnidium	1		0
Olea europaea var. sylvestris	6		20
Pistacia lentiscus	3		0
Pyrus bourgaeana	1		0
Quercus suber	1		5
Rubus ulmifolius	3		7
Stauracanthus genistoides	31		17

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Number of samples (feces, seeds) collected in each study plot, the number of seeds found for each plant species, as well as the number and species of bird recorded perching on C. humilis.

Every target C. humilis was checked for bird feces and regurgitations by carefully checking the palm foliage surface. We also evaluated whether seeds arrive at open spaces without palms. To this aim, we checked for the presence of bird feces and regurgitations in an open area associated with each focal C. humilis. These areas were of similar surface and mostly located in bare soils with scarce vegetation (mainly grasses) and 3–4 m from the associated C. humilis. Every found excrement and regurgitated seed was collected and stored inside of an individual Eppendorf tube. In the lab, feces were dried to make their handling easier. Once dried, every sample was checked for seeds by crumbling the excrement and looking for hard matter, either of vegetable (seeds, bark) or animal (elytra and other arthropod parts) origin. Found seeds were identified at the species level using images of a reference collection (Fig 3), considering its shape, size and the surface design. All collected seeds (N = 529) were positively identified.

Fig 3 — (A) Bird excrement on a leaf of *Chamaerops humilis* in the early-successional plot. Seeds of (B) *Asparagus aphyllus*, (C) *Daphne gnidium*, (D) *Olea europaea* var. *sylvestris*, (E) *Phillyrea angustifolia*, (F) *Pistacia lentiscus*, and (G) *Rubus ulmifolius*. (Photo credit: Pedro J. Garrote).

To assess the potential selection by birds of particular traits of C. humilis individuals, we measured the following palm variables: gender (male, female, undetermined), size (height, area and volume), presence and richness of beneficiary woody species associated with them and beneficiary height (< 25 cm, 25–100 cm, > 100 cm). The beneficiary species were woody plants that grow under dwarf palms and whose branches appear from the upper surface of these. These species often benefit from C. humilis due to microclimatic improvement and protection against herbivory [42].

Spatial analyses

Aggregation of C. humilis used as perches within the overall pattern of C. humilis

Every C. humilis was characterized with its spatial location and a mark (presence/absence of bird feces in this case). To find out if C. humilis used as perches by birds (i.e. receiving bird feces) show a spatial pattern (aggregated, isolated) or they instead are randomly distributed we used qualitatively marked point patterns techniques and the random labelling null models to evaluate lack of any spatial structure. The random labelling null model consists in giving the mark “with feces” or “without feces” over all C. humilis (having or not feces) randomly, conducting a total of 199 simulations [38].

In order to quantify the spatial pattern of C. humilis used as perches within the overall pattern of C. humilis we used mark connection functions [43–45] as summary statistics [38]. Whether C. humilis contained feces they were assigned with a mark of value 1 and a mark of value 0 if they had no feces. The mark connection function p_ij(r) gives the probability that two C. humilis, separated by a distance r, the first is type i (i.e. with feces) and the second is type j (without feces).

Finally, to test if C. humilis with feces are located in areas of overall high density of neighbouring C. humilis (with feces or without them) we used the test statistic g_i,i+j(r)–g_j,i+j(r) [44], which consist in comparing the density of C. humilis (i + j) around C. humilis with feces (type i) with the density of C. humilis (i + j) around C. humilis without feces (type j). Under random labelling, the expected value for this statistic is zero: in case that feces tend to be delivered in palm aggregations we expected g_i,i+j(r) > g_j,i+j(r) and, if not, if there is an isolation of feces, the we expected g_i,i+j(r) < g_j,i+j(r).

To test the fit of data with the point process and departures from the null model, we conducted 199 simulations (for every analysis) of the fitted point processes and estimated envelopes with an approximate error rate of α = 0.05 [46] which are the fifth lowest and highest values of the summary statistics of the simulated point process. Observed values above the top or below the bottom simulation envelopes indicate higher or lower than expected spatial aggregation, respectively. Observed values within the simulation envelopes indicate a level of spatial aggregation compatible with the stochasticity of the point process model. For all point pattern analyses, we used the grid-based software Programita [47].

Aggregation of C. humilis receiving dispersed seeds within the overall pattern of C. humili

To assess if C. humilis containing (feces with) dispersed seeds were randomly distributed within the pattern of all C. humilis (with and without seeds) or they follow a particular spatial pattern (aggregation, dispersion), we also used qualitatively marked point pattern techniques and the random labelling null model to represent lack of any spatial structure. The same process and analysis were conducted as in the previous case but, in this occasion, the used mark was the presence (1) or absence (0) of seed in each individual C. humilis. In parallel, these same analyses were carried out but excluding the Rubus’ seeds since their great number could distort the spatial pattern for the presence of seeds on C. humilis (see S2 File and S2 Fig). Since results were rather consistent whether we considered or not Rubus’s seeds, here we provide the results when all seed species are included.

Association of the number of dispersed seeds on C. humilis

To find out whether the number of dispersed seeds within bird feces deposited on C. humilis has a spatial association among different C. humilis we used quantitative marked point patterns techniques and the random labelling null model to represent lack of any spatial structure.

To quantify potential spatial associations in the number of seeds on different C. humilis we used the univariate mark correlation function as summary statistic [38, 43, 47, 48], ergo we wanted to find out if closer C. humilis had a higher number of seeds than isolated ones. In addition to its location, each C. humilis was characterized by a quantitative mark: the number of dispersed seeds of any species.

Mark correlation functions are based on pairs of study units (in this case C. humilis individuals) and the idea of estimating the mean value of a test function t(m_i, m_j) of the two marks m_i and m_j, taken over all the ordered pairs i-j of C. humilis which have interpoint distances of r ± h, being h the parameter bandwidth, which must be wide enough to produce a sufficient number of pairs in each distance class r but small enough to reveal significant biological detail [43, 49]. From all possible test functions t(m_i, m_j) [43], we selected the following three:

(i) The r-mark correlation function k_m1. (r) which is based on the test function: t(m_i, m_j) = m_i. k_m1. (r) > 1 indicates that the number of seeds on C. humilis that have neighbouring C. humilis at distance r is larger than the average of seeds, showing a positive effect of C. humilis aggregation on seed number. By contrast, if k_m1. (r) < 1, it would indicate a negative effect of aggregation and a positive effect of isolation of C. humilis on seed number [49]. Finally, if k_m1. (r) ~ 1, indicates that the number of seeds is not affected by the distance to C. humilis individuals.
(ii) Another mark correlation function was calculated to characterize the spatial covariance in number of seeds of two C. humilis separated by distance r. This test function is known as Schlather’s: t(r, m_i, m_j) = [m_i—μ(r)][(m_j—μ(r)] which results in a Moran’s I like summary statistic I_mm(r), a spatial variant of the Pearson correlation coefficient between the variables m_i and m_j defined by the ordered i-j pairs of C. humilis separated by distance r ± h.
(iii) Lastly, we used a function that relates the number of seeds on a C. humilis directly to the density of neighbouring C. humilis, called “density correlation function” [49]: C_m,K(r). This function estimates the Pearson correlation coefficient between the number of seeds m_i and the number of neighbours within distance r, based on the following equation: t(r, m_i, K_i) = [m_i = μ][(λK_i(r)—λK_i(r)]. Where m_i is the number of seeds of the focal C. humilis i, λ is the overall density of C. humilis in the study area, μ is the mean number of seeds of the population, λK_i(r) is the number of neighbours around the focal C. humilis i within distance r for all C. humilis.

To test whether the data show spatial correlation, the observed values of the three functions mentioned above were contrasted to the data obtained from simulations of a null model without spatial correlation in the marks. The null model consisted in shuffling randomly the marks (number of seeds) over all C. humilis, conducting a total of 199 simulations. These simulations were also useful to estimate the simulation envelopes for the three functions, being the fifth highest and lowest values of the summary statistics among all simulations of the null mode [38, 49].

Effect of palm traits

To analyse how our response variables (presence of bird feces, presence of dispersed seeds and number of dispersed seeds) were influenced by the size (height, area and volume) and gender (male, female) of C. humilis individuals, as well as by the presence (and height: < 25 cm, 25–100 cm, >100 cm) of beneficiary species, three sets of generalized linear models (GLMs) were fitted per study plot.

Model 1 assessed the effect of palm traits on the likelihood of presence of bird feces, Model 2 evaluated the probability of finding dispersed seeds depending on such characteristics and Model 3 appraised the number of seeds based on those characteristics. Both Model 1 and Model 2 have a binary response variable (presence = 1, absence = 0), and thus were fitted with a binomial distribution and a logit link. Finally, Model 3, was fitted with a Poisson distribution with logit link.

A set of competing models were fitted and the best candidate model was selected based on Akaike’s Information Criterion (AIC), allowing to compare different hypothesis and know their supportive level on the data by weighting them (AICc; [50]). All analyses were performed in R 4.0.3 statistical software [51]. Additionally, these same models were carried out but using the interaction between C. humilis Height (m) and Area (m²) instead of the variable Volume (m³). Results were rather consistent with those from the previous analysis (see S2 Table).

Results

Overall patterns

We studied total of 109 C. humilis in the early-successional plot, from which were collected 705 bird feces and 28 seeds in 2019 and 206 bird feces and 16 seeds in 2020 (Fig 4). In the late-successional plot, we monitored 180 C. humilis, 1560 feces and 340 seeds in 2019, and 527 feces and 145 seeds in 2020. Nevertheless, not all dispersed seeds were contained within the feces since a small fraction was regurgitated by the birds. Six shrub species were identified among the collected seeds: A. aphyllus, D. gnidium, O. europaea var. sylvestris, P. angustifolia, P. lentiscus and R. ulmifolius. Finally, a large fraction of C. humilis acted as perch for birds and contained their feces: 42.2% (2019) and 37.6% (2020) in the early-successional plot and 43.9% (2019) and 27.8% (2020) in the late-successional plot (Table 1).

Fig 4 — (A) C. *humilis* in the early-successional plot with (black solid points) and without (white circles) bird feces or regurgitations. (B) C. *humilis* in the early-successional plot with (black solid points) and without (white circles) dispersed seeds. (C) C. *humilis* in the late-successional plot with (black solid points) and without (white circles) bird feces. (D) C. *humilis* in the late-successional plot with (black solid points) and without (white circles) dispersed seeds.

Besides, most C. humilis had beneficiary woody plants growing within them. In the late-successional plot and the early-successional plot 104 out of 180 individuals (57.78%) and 71 out to 109 (65.14%) had beneficiary plants, respectively. A total of nine different beneficiary species were found, all of them present in the early-successional plot but just five were recorded in the late-successional plot (Table 1).

Spatial patterns

Aggregation of C. humilis used as perches within the overall pattern of C. humilis. Analysis of how C. humilis used as perches by birds (i.e. receiving bird feces) were distributed within the overall pattern of C. humilis showed the following results. In the early-successional plot, the probability that two C. humilis, separated by a distance r, both used as perches (statistic p₁₁(r)), fall within the expectation of random labelling (Fig 5A). The probability that two separated C. humilis, with just one comprising feces (statistic p₁₂(r)), was included within the simulation envelops generated by random labelling (Fig 5C). Finally, the observed density of neighbouring C. humilis (regardless of having feces or not; statistic g_i,i+j(r)–g_j,i+j(r)) around C. humilis with feces was within the simulation envelops generated by a random labelling mode (Fig 5E). Thus, in the early-successional plot, the observed probabilities described by the three statistics were within the envelops generated by random labelling models, which indicates they are compatible with the stochasticity of the process model.

Fig 5 — (A, B) The mark connection function p₁₁(r) gives the conditional probability that, from two C. *humilis* that are separated by distance r, both are type 1 (i.e., with feces). (C, D) The mark connection function p₁₂(r) gives the conditional probability that, from two C. *humilis* that are separated by distance r, the first is type 1 (i.e., with feces) and the second is type 2 (i.e., without feces). (E, F) The test statistic g_1,1+2(r)—g_2,1+2(r) compares the density of C. *humilis* (i.e., 1+2) around C. *humilis* with feces (i.e., type 1) with the density of C. *humilis* (i.e., 1+ 2) around C. *humilis* without feces (i.e., type 2). The expected mark connection function statistics (gray line) and the corresponding simulation envelopes (black lines), being the fifth lowest and highest values of the functions created by 199 simulations under random labelling, are also shown.

On the contrary, in the late-successional plot, the probability that two C. humilis separated for distances 1-6m, both having feces (p₁₁(r) statistic), was lower than the expectation under random labelling. The bivariate p₁₂(r) showed that C. humilis with and without feces were further away than expected under random labelling up to scales of 6m (Fig 5D). Finally, the density of neighbouring C. humilis (having or not feces) around C. humilis with feces was significantly lower than expected by random labelling for distances up to scales of 7m (Fig 5F). Overall, these results indicate a tendency by frugivorous birds in the late-successional plot towards using and defecating in isolated C. humilis individuals.

Distribution of C. humilis receiving dispersed seeds within the overall pattern of C. humilis

In the early-successional plot, the probability p₁₁(r), where two C. humilis separated by distance r, both having seeds, was contained within the envelopes of random labelling for all spatial scales (Fig 6A). The bivariate p₁₂(r), the probability for two neighbouring C. humilis, one with seeds and other without them, was also contained between random labelling’s envelopes (Fig 6C). Finally, the test statistic g_1,1+2(r)—g_2,1+2(r) shows that the density of neighbouring C. humilis around C. humilis receiving seeds did not differ from the mean C. humilis density. (Fig 6E).

Fig 6 — (A, B) The mark connection function p₁₁(r) gives the conditional probability that, from two C. *humilis* that are separated by distance r, both are type 1 (i.e., with seeds). (C, D) The mark connection function p₁₂(r) gives the conditional probability that, from two C. *humilis* that are separated by distance r, the first is type 1 (i.e., with seeds) and the second is type 2 (i.e., without seeds). (E, F) The test statistic g_1,1+2(r)—g_2,1+2(r) compares the density of C. *humilis* (i.e., 1+2) around C. *humilis* with seeds (i.e., type 1) with the density of C. *humilis* (i.e., 1+ 2) around C. *humilis* without seeds (i.e., type 2). The expected mark connection function statistics (gray line) and the corresponding simulation envelopes (black lines), being the fifth lowest and highest values of the functions created by 199 simulations under random labelling, are also shown.

Results in the late-successional plot substantially differed from results from the early-successional plot. The probability of two C. humilis separated by distance r, having both seeds (p₁₁(r) statistic), was similar to expected of random labelling for all spatial scales (Fig 6B). However, the probability for two neighbouring C. humilis, just one of them with seeds (p₂(r) statistic), was significantly lower (P = 0.01) that the obtained by using random labelling for distances up to 6 m, between 12 and 29 m and higher than 41 m (Fig 6D). Neighbourhood density of C. humilis around C. humilis receiving seeds was significantly lower (P = 0.005) than the mean C. humilis density at scales of 1 to 6 m (Fig 6F).

In short, the analysis of how C. humilis with seeds were distributed within the overall pattern of C. humilis showed that C. humilis with seeds were randomly distributed in Matagordas (Fig 6A, 6C and 6E) while, in the late-successional plot, C. humilis with seeds were spatially isolated at small spatial scale (Fig 6D and 6F).

Distribution of the number of dispersed seeds across C. humilis

The observed r‐mark correlation function for the number of seeds was included within the simulation envelop for all scales, indicating no relationship between distance among individual C. humilis and the number of dispersed seeds neither in the early-successional plot (P = 0.95, Fig 7A) nor in the late-successional plot (P = 0.31, Fig 7B). Similarly, the Schlather’s correlation function did not show a correlation between number of seeds and distance among individuals at any spatial scales, neither in the early-successional plot (P = 0.22, Fig 7C) nor in the late-successional plot (P = 0.22, Fig 7D). Finally, the density correlation function did not indicate correlation between the number of seeds and the density of C. humilis at any scale neither in the early-successional plot (P = 0.35, Fig 7E) nor in the late-successional plot (P = 0.35, Fig 7F).

Fig 7 — (A, B) The r‐mark correlation function describes the mean number of seeds (m_i) on a C. *humilis* at distance r of another C. *humilis*. (C, D) Schlather’s correlation function quantifies the correlation between the number of seeds on two different C. *humilis* separated by distance r. (E, F) Density correlation function assesses the correlation between the number of seeds and the number of neighbours located at a distance r. The expected mark connection function statistics (gray line) and the corresponding simulation envelopes (black lines), being the fifth lowest and highest values of the functions created by 199 simulations under random labelling, are also shown.

Effect of palm traits

We found that C. humilis in the early-successional plot were on average (8.80 m²) smaller than in the late-successional plot (15.26 m²). Also, the richness of beneficiary species beneath C. humilis was slightly lower in the early-successional plot than in the late-successional plot, with 0.89 and 1.07 beneficiary species per individual, respectively.

For the early-successional plot, the best model (AIC = 133.97) showed that presence of bird feces on C. humilis were positively related to their height and area, but negatively to volume, although none of these variables were found significant (Table 2. Model 1). The best model for the late-successional plot (AIC = 196.63) indicated that presence of bird feces on C. humilis was higher in male than females and positively influenced by palm area, but negatively to the richness of beneficiary species contained within them. Nevertheless, only the palm area was found significant (P < 0.001).

Table 2. GLM carried out to analyze the palm traits in the early-successional plot.

Explanatory variable	Competing models		β	SE	AICc	ΔAIC	Weighted AIC
*Model 1*
Presence of Bird Feces	Height (m) + Area (m²) + Volume (m³)				133.97	0	0.62
		Intercept*	-4.586	2.244
		Height (m)	5.930	3.513
		Area (m²)	0.411	0.219
		Volume (m³)	-0.450	0.282
	Gender + Height (m) + Area (m²) + Volume (m³)				135.67	1.7	0.27
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness				137.54	3.57	0.10
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				143.11	9.14	0.01
Deviance = 90.343
*Model 2*
Presence of Dispersed Seeds	Gender + Height (m)				96.343	0	0.05
		Intercept*	-4.969	1.441
		Gender (Male)	0.915	0.557
		Height (m)*	4.294	1.837
	Gender + Height (m) + Volume (m³)				98.21	1.87	0.02
	Gender + Height (m) + Area (m²) + Volume (m³)				99.03	2.69	0.01
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness				100.73	4.39	< 0.01
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				107.56	11.2	< 0.01
Deviance = 126.52
*Model 3*
Number of Dispersed Seeds	Gender + Height (m) + Volume (m³)				191.41	0	0.11
		Intercept*	-5.988	1.153
		Gender(Male)*	0.822	0.354
		Height (m)*	7.737	2.033
		Volume (m³)*	0.134	0.065
	Gender + Height (m) + Area (m²) + Volume (m³)				192.77	1.36	0.06
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness				194.47	3.06	0.02
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				196.18	4.77	0.01
Deviance = 133.75

Open in a new tab

Summary of fitted parameters and models employed to analyse the presence of bird feces (model 1), the presence of dispersed seeds (model 2) and the number of dispersed seeds (model 3) on C. humilis in the early-successional study plot. Competitive models are ranked from the lowest AICc value (best model) to the highest one, being significant variables indicated with asterisks (*).

Presence of dispersed seeds in the early-successional plot depended on C. humilis gender and height (Table 2. Model 2), according to the best model obtained (AIC = 96.343). Nonetheless, only the height was significant (P < 0.05) with larger C. humilis individuals having a higher number of dispersed seeds. In the late-successional plot, the best model obtained (AIC = 137.98) showed that height and richness of beneficiary species had a positive effect on the number of dispersed seeds, although just the last one was significant in this case (P < 0.01) (Table 3. Model 2).

Table 3. GLM carried out to analyze the palm traits the late-successional plot.

Explanatory variable	Competing models		β	SE	AICc	ΔAIC	Weighted AIC
*Model 1*
Presence of Bird Feces	Gender + Area (m²) + Richness				196.63	0	0.54
		Intercept*	-0.776	0.304
		Gender (Male)	0.5583	0.352
		Area (m²)*	0.089	0.024
		Richness	-0.485	0.266
	Gender + Area (m²) + Volume (m³) + Richness				197.88	1.25	0.29
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness				199.49	2.86	0.13
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				201.76	5.13	0.04
Deviance = 188.63
*Model 2*
Presence of Dispersed Seeds	Height (m) + Richness				137.98	0	0.62
		Intercept*	-3.383	0.549
		Height (m)	0.480	0.273
		Richness*	1.971	0.731
	Height (m) + Volume (m³) + Richness				139.86	1.88	0.24
	Height (m) + Area (m²) + Volume (m³) + Richness				141.64	3.66	0.10
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness				143.5	5.52	0.04
	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				147.44	9.46	< 0.01
Deviance = 131.98
*Model 3*
Number of Dispersed Seeds	Gender + Height (m) + Area (m²) + Volume (m³) + Richness + Beneficiary height (cm)				1273.09	0	1
		Intercept*	-2.823	1.078
		Gender (Male)*	1.802	0.127
		Height (m)*	-1.946	0.458
		Area (m²)*	-0.114	0.014
		Volume (m³)*	0.134	0.014
		Richness*	0.957	0.093
		Beneficiary height (25-100cm)	0.7794	1.034
		Beneficiary height (>100cm)*	2.59102	1.022
Deviance = 1155.7

Open in a new tab

Summary of fitted parameters and models employed to analyse the presence of bird feces (model 1), the presence of dispersed seeds (model 2) and the number of dispersed seeds (model 3) on C. humilis in the late-successional study plot. Competitive models are ranked from the lowest AICc value (best model) to the highest one, being significant variables indicated with asterisks (*).

According to the best model in the early-successional plot (AIC = 191.41), male C. humilis had a higher number of dispersed seeds than females (P < 0.05) and height had a positive and significant (P < 0.001) influence on the number of seeds found on C. humilis. Palm volume had a negative effect on the number of seeds (P < 0.05) (Table 2. Model 3). Finally, in the late-successional plot, just one model was fitted (AIC = 1273.09). This model predicted: (i) a negative relationship between height and area of C. humilis and the number of dispersed seeds (P < 0.0001); (ii) a higher number of dispersed seeds in male C. humilis than in females (P < 0.0001); (iii) a positive relationship between C. humilis volume and the number of dispersed seeds (P < 0.0001); (iv) a positive relationship between the richness of beneficiary species in C. humilis and the number of dispersed seeds (P < 0.0001); and (v) a higher number of dispersed seeds in C. humilis holding tall (> 100 cm in height) beneficiary woody individuals as compared to both small (< 25 cm) and intermediate (25–100 cm) beneficiary individuals (P < 0.05; Table 3, Model 3).

Discussion

The role of pioneer plants acting as perches for seed dispersers is crucial for the restoration of many human-disturbed habitats by increasing seed arrival and eventually seedling establishment [52–55]. Using a spatially explicit approach, we detected a random spatial structure in both the number of visits (bird feces) and the dispersed seeds found on C. humilis in one study plot (the early-successional) and an aggregated pattern in the other one (the late-successional). Frugivorous birds tended to disperse seeds into a small number of C. humilis individuals, usually male and large-sized ones, that acted as “hotspots” of seed arrival. Our study also revealed that the species of dispersed seeds partially matched the woody beneficiary species growing inside C. humilis, reinforcing the idea that this palm species plays a key role in the restoration of disturbed habitats.

Widespread perching effect by C. humilis

Considering that our sampling period did not take place throughout the year and that an unknown fraction of the bird feces presents in target C. humilis individuals surely went unnoticed, the data obtained could be considered as a hint of how widespread the "perching” effect in both study plots. Therefore, the high presence of (frugivorous) bird feces and dispersed seeds in both study plots is noteworthy.

Besides, it is apparent that some seeds can emerge seedlings beneath C. humilis, since all seeds collected belonged to beneficiary woody species found within C. humilis. Nevertheless, we did not find seeds of the beneficiary species C. salviifolius, P. bourgaeana, Q. suber and S. genistoides, which also are frequently associated with C. humilis. Most of these plant species are seldom dispersed by birds. Other animals are more likely to disperse them, such as insects for C. salviifolius and S. genistoides seeds [56–58] or mammals, such as ungulates (red deer, wild boars, domestic cattle) and carnivores (Eurasias badger, red fox) for P. bourgaeana seeds [59]. Therefore, the presence of these woody species associated with C. humilis reveals that it does not attract just bird-dispersed plants but also mammal and insect-dispersed plants, accentuating its role in habitat restoration.

Spatial patterns of the perching effect

Our study has revealed different spatial patterns in both study plots at the three target organizational levels studied: (i) C. humilis receiving bird feces, (ii) C. humilis receiving (feces with) dispersed seeds, and (iii) number of dispersed seeds arriving to C. humilis.

No spatial pattern was found in the early-successional plot, where the distribution of C. humilis did not seem to play a decisive role in attracting frugivorous birds. By contrast, in the late-successional plot, where isolated palms were more frequent than in the early-successional plot, there was strong evidence that birds preferred isolated C. humilis, at least for those separated from conspecifics by a distance up to 7 m. Aggregated perches could be found attractive for seed dispersers and, therefore, more visited by them [60], since they would act as shelters against predators [61]. This premise has been used for designing ecological restoration and conservation actions in mixed ecosystems, where trees or other woody plants, acting as perches and nurses, are planted following aggregated spatial patterns [62–65]. However, by concentrating frugivorous activity to aggregated planted trees, seed dispersal could be limited [16, 55]. Therefore, our results from the late-successional plot supporting the role of isolated perches diverge from the most widespread tendency in ecological restoration of aggregating trees and shrubs during revegetation efforts [65].

Spatial patterns of perching effect differed between study plots. On the one hand, these differences could be attributed to the changing distance that frugivorous birds must fly between the main seed source area (Mediterranean scrubland) and our study plots where target C. humilis individuals are located. This distance is longer in the early-successional plot (up to 350 m) than in the late-successional plot (150–200 m). Besides, it seems reasonable to expect that birds select C. humilis located on the edge of the plot, since these individuals are closer to the Mediterranean scrubland and thus allow birds to move between habitats with a minimal consumption of energy. On the other hand, both plots are open habitats and have been intensively disturbed by humans in the past, but with some decades apart [16, 41]. Thus, study plots are in different stages of ecological succession and the vegetation surrounding them is different too. For instance, in the early-successional plot there are more scattered trees (mostly Q. suber and O. europaea var. sylvestris) than in the late-successional plot. The reduced number of feces and seeds and the lack of spatial patterns found in the early-successional plot could relate to the bird’s intensive usage of such scattered trees. A recent study has shown that in the later-successional site the “nursing” effect of C. humilis may be diluted among different shrub species [4], since the landscape is dominated by shrub-encroached communities. The “perching” effect of C. humilis, however, seems to follow the opposite trend, being enhanced in the most shrub-encroached landscape (i.e. Reserva) probably because of the few available trees for perching.

Interestingly, we found that most of dispersed seeds were concentrated in a small number of C. humilis individuals that acted as “hotspots” of seed arrival. For example, in the late-successional plot there was a single large C. humilis individual receiving 47.4% of the total seeds found in that plot (N = 485). These results are supported by previous evidence that a small number of individual trees can play an important role in habitat restoration by altering the movements of seed dispersers and thus increasing influx of animal-dispersed seeds [16, 55]. Features (other than spatial patterns) that make particular C. humilis individuals hotspots of seed arrival are discussed below.

Palm trait’s influence on perching effect

This investigation identified some features that made particular C. humilis attractive “perching” sites for frugivorous birds and, therefore, hotspots for seed arrival. However, this pattern was found only in the late-successional plot, and not in the early-successional plot. In the late-successional plot, larger C. humilis individuals received more seeds as compared to small ones. The greater surface of large individuals could attract more birds since it implies a greater number of entry points to C. humilis interior, where the bird could be safe from predators and adverse weatherly conditions (e.g. high temperatures, wind).

The use of C. humilis as “perching” site by birds does not necessarily implies seed arrival since not all recorded birds are typical seed dispersers [66]. However, we sampled during peak of the seed dispersal season, time when most recorded birds change their diet into a more fruit-based one. For instance, it has been reported that P. ochruros, S. atricapilla and S. malenocephala are able to quickly change their diet when fleshy fruits become available, while other species such as S. rubicola show a more gradual change to a frugivorous diet [67, 68]. Also, S. unicolor, P. ochruros, P. pica, and S. rubicola has been reported as fruit-eater, although in lesser quantities [69–73]. Therefore, although not all recorded bird species contribute equally to seed dispersal, fleshy fruits represent a variable fraction of their diets during the seed dispersal season.

Secondly, the preference of taller C. humilis by frugivorous birds could relate to their own requirements as well as to characteristics of the surrounding landscape [74]. Taller C. humilis could suppose safer places since they would provide greater visual fields to birds to spot potential predators. Also, taller perches are likely better sites to take flight towards other habitats (e.g. the Mediterranean scrubland) adjacent to the studied site, which may be more suitable habitats for them [64, 75, 76].

The detected positive effect of richness of beneficiary species within C. humilis in the late-successional plot could be related to some of them producing fleshy fruits (e.g. Rubus ulmifolius, Asparagus aphyllus), acting thus as an additional attractant for frugivorous birds [77–79]. Richness of beneficiaries was also found positively related to the number of seeds found on C. humilis, which is likely a consequence of the increased number of frugivorous bird visits. Additionally, beyond the fact of bearing fleshy fruits, the own beneficiary species could be used as a perch and thus attract birds. Therefore, a similar reasoning explained earlier about how C. humilis height influences seed dispersal, could be applied for the revealed positive effect of height of beneficiary plants. Finally, it seemed that male C. humilis were more likely to receive dispersed seeds than females. We speculate that male C. humilis could be selected by birds over females because the former have a lower associated predation risk. Females C. humilis produce fleshy fruits that are too large for birds, but they are often eaten by medium-sized carnivores such as the Eurasian badger and the red fox [33]. Although these mammals are mainly nocturnal, their presence likely prevents birds from using female C. humilis in fruit as shelter at nighttime, and thus may dissuade them at daytime too. Therefore, the use of C. humilis in ecological restoration should follow a balance between male and female plants. Male plants would attract preferably birds that would disperse small-seeded woody species present in the surrounding area, while female plants would attract medium-sized carnivores and ungulates that would mostly disperse large-seeded species such as P. bourgaena and C. humilis.

In summary, taller and isolated male C. humilis with a higher diversity of beneficiary species seemed to be the most suitable individuals for attracting frugivorous birds and, therefore, received higher number of dispersed seeds. However, this pattern was not entirely confirmed in the early-successional plot, likely because of a much smaller sample sizes (i.e. lesser numbers of both C. humilis used as perches and of dispersed seeds).

Conclusions and implications for ecological restoration

In the last 30 years, restoration ecology has undergone considerable development thanks to the emerging new tools and techniques that facilitate the retrieval of biological properties of disturbed habitats [80]. Our study plots are a good representation of Mediterranean old fields, which have been targets for habitat restoration [5, 16]. Previous studies have demonstrated the value of C. humilis in these programs since it facilitates recruitment of numerous woody species dispersed by frugivores [4, 36]. Here, we have demonstrated that C. humilis also exerts a marked “perching” effect, crucial in restoration and ecological succession [27, 52, 81, 82]. The combination of artificial and natural perches with nurse plants could increase the seed arrival and recruitment leading to nucleation processes around them [4, 19, 20]. In this sense, to our knowledge, this study represents the first spatially explicit assessment of the relationship between natural perches and seed arrival via frugivorous birds in Mediterranean human-disturbed landscapes. Our results could be used by managers to decide, for example, whether particular areas are adequate to promote seed arrival using natural or artificial perches.

Our finding in the late-successional plot indicating that dispersed seeds are concentrated in a few C. humilis individuals, which tend to be isolated from the rest, breaks surprisingly with the general trend of revegetating under an aggregation design (e.g. [64, 65, 83]. However, our results are in agreement with Fedriani and collaborators [16] whose simulated P. bourgaeana seed dispersal into human-altered habitats within the Doñana National Park and found that planting isolated trees was the most efficient strategy to enhance seed arrival. Though further research is needed to evaluate the pervasiveness of our findings, the strategy of using aggregated perches for increasing seed arrival and habitat restoration likely should not be advocated under all ecological circumstances.

To conclude, this investigation supports previous studies about the importance of the pioneer C. humilis for the restoration of human-disturbed Mediterranean landscapes. We prove for the first time its key role as natural perch, an ecological function that, though it is shared with some woody plants, is especially relevant in early stages of ecological succession when few pioneer species occur. Birds tended to disperse seeds into a small number of C. humilis individuals (usually isolated male and large-sized ones) that acted as “hotspots” of seed arrival. Thanks to the double role of C. humilis, which attracts frugivorous birds that deliver considerable numbers of seeds of late-successional woody species and provides improved conditions for seedling emergence and survival, it is likely to become a successful tool for ecological restoration in many habitats of the western Mediterranean basin.

Supporting information

S1 File. Cluster analysis.

Technical details concerning the cluster analysis.

(DOCX)

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S2 File. Spatial analysis excluding Rubus’ seeds.

(DOCX)

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S1 Table. Summary of the results of the C. humilis distribution fitted with the Thomas cluster process.

(DOCX)

Click here for additional data file.^{(12.9KB, docx)}

S2 Table. GLM carried out to analyze the palm traits in the early-successional plot.

A General Linear Model (GLM) was carried out with the interaction between C. humilis Height (m) and Area (m²) as a new variable instead of the C. humilis Volume (m³). The results found are pretty similar to the ones obtained by using the variable Volume (m³) in both study plots. Thus, we decided to maintain the initial model.

(DOCX)

Click here for additional data file.^{(15.7KB, docx)}

S3 Table. GLM carried out to analyze the palm traits in the late-successional plot.

A General Linear Model (GLM) was carried out with the interaction between C. humilis Height (m) and Area (m2) as a new variable instead of the C. humilis Volume (m3). The results found are pretty similar to the ones obtained by using the variable Volume (m3) in both study plots. Thus, we decided to maintain the initial model.

(DOCX)

Click here for additional data file.^{(21KB, docx)}

S1 Fig

Univariate cluster analysis for Chamaerops humilis in the early (A, C, E, G) and late-successional study plots (B, D, F, H). (A, B) Pair correlation function g(r). (C, D) L-function L(r). (E, F) Spherical contact distribution H_S(r). (G, H) Nearest neighbor distribution function D1(r). The expected mark connection function statistics (gray line) and the corresponding simulation envelopes (black lines), being the fifth lowest and highest values of the functions created by 199 simulations of the null model, are also shown.

(DOCX)

Click here for additional data file.^{(131.7KB, docx)}

S2 Fig. Analysis of feces with seeds (excluding Rubus) in the late-successional study plot using mark connection functions as summary statistics.

(A) The mark connection function p₁₁(r) gives the conditional probability that, from two C. humilis that are separated by distance r, both are type 1 (i.e., with seeds). (B) The mark connection function p₁₂(r) gives the conditional probability that, from two C. humilis that are separated by distance r, the first is type 1 (i.e., with seeds) and the second is type 2 (i.e., without seeds). (C) The test statistic g_1,1+2(r)—g_2,1+2(r) compares the density of C. humilis (i.e., 1 + 2) around C. humilis with seeds (i.e., type 1) with the density of C. humilis (i.e., 1 + 2) around C. humilis without seeds (i.e., type 2). (D, E, F) Mark correlation functions to evaluate a potential spatial structure in the number of dispersed seeds (excluding Rubus). (D) The r‐mark correlation function describes the mean number of seeds (mi) on a C. humilis at distance r of another C. humilis. (E) Schlather’s correlation function quantifies the correlation between the number of seeds on two different C. humilis separated by distance r. (F) Density correlation function assesses the correlation between the number of seeds and the number of neighbours located at a distance r. The expected mark connection function statistics (gray line) and the corresponding simulation envelopes (black lines), being the fifth lowest and highest values of the functions created by 199 simulations under random labelling, are also shown.

(DOCX)

Click here for additional data file.^{(134.1KB, docx)}

Data Availability

All data files are fully available at: https://figshare.com/articles/dataset/PerchigEffectDwarfPalm_xlsx/19642446.

Funding Statement

This work was supported by the Portuguese Foundation for Science and Technology to PJG (SFRH/BD/130527/2017) and by a grant of the Spanish Ministry of Education and Science to JMF (PGC2018-094808-B-I00). Logistic and technical support was provided by ICTS-RBD. The authors acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0273311.r001

Decision Letter 0

Karen Root

25 Feb 2022

PONE-D-22-01669Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L.PLOS ONE

Dear Dr. González-García,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

This paper examines an interesting restoration question about the role of perch plants for seed dispersal in disturbed environments. It addresses an important conservation issue but the paper needs substantive improvements to be suitable for publication, including editing for language issues. The questions are clearly delineated, although, as the reviewers suggest there is some detail missing in the description of the design and initial predictions. The results are interesting and well organized but need more clarification, as Reviewer #2 details.

The discussion, though, needs substantial revision to increase clarity and improve the interpretation of your results, especially in terms of language. It contains many awkwardly worded sentences that are challenging to understand (e.g., lines 459-462; 465-467; 493-497; 508-511; 550-552; 565-566; 594-596) and/or use poor grammar (e.g., lines 268-269; 502-503; 536-537; 559-561). Some of these issues could be minimized if you use more active rather than passive voice.

In particular, it will be important to address the concerns of the both of the reviewers who highlight a number of areas that need further exploration. Reviewer #1 has some concerns about the foraging and movement ecology of the dispersers and the potential impact on the seed dispersal patterns as well as the large differences in the types of seeds potentially dispersed. Please also note that Reviewer #1 has some specific questions that should be addressed to improve clarity, particularly in the study design and motivations. Reviewer #2 also provides some valuable recommendations for each section and identifies a number of places where more explanation or revision is needed. Some additional issues are identified below:

Line 63: “template” should be “temperate”

Line 99: The use of the term “beneficiary” requires some type of description/definition or a reference source. What characteristics define this group and is it context-dependent?

Line 232: Why 199 simulations? It seems like a rather arbitrary number. Is this based on some initial modeling or preliminary results?

Line 255: “that” should be “than”

Both reviewers provide detailed suggestions in how to improve the manuscript and reframe the paper to make it better highlight the strengths. With substantial improvements this paper could make a welcome contribution to the restoration literature.

Please submit your revised manuscript by Apr 11 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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Reviewer #1: Partly

Reviewer #2: Partly

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Reviewer #2: Yes

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Reviewer #2: Yes

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Reviewer #1: Although there is a lot of consideration on the use of artificial perches in restoration, the role of natural perches deserves more investigation, especially in a poorly studied biome under this perspective, as is the case with Mediterranean Europe. In this regard, the authors provide an important dataset based on field observations and fine spatial analyses, which represents a great contribution to the restoration of that particular habitat.

Despite their efforts to explain the different patterns found between the two study sites (Mastasgordas and Reserva), I think this attempt was a bit confused, perhaps because there may be underlying causes not fully investigated by the authors. I would put this question in the perspective of the field data and not in the analysis itself. One underlying problem may be the unbalanced frequency of birds and seeds in the two areas. From the nine bird species recorded, six are reputed insectivores and just three can be considered omnivores that can take significant amounts of fruit in their diets (https://esajournals.onlinelibrary.wiley.com/doi/abs/10.1890/13-1917.1). These three omnivore species performed more than 50% of the visits recorded in the two areas and probably deposited more seeds per visit beneath the palms than the other ones. Special attention should be paid to the foraging and movement patterns of these three omnivores, since they may account for the general pattern of the seed rain and, perhaps, provide sound explanations for these patterns.

Another point addresses the plant composition and fruit types between the two areas. Rubus ulmifolius is the only recorded fruit consumed that is a functional berry, containing dozens of seeds. The other plant species are single-seeded drupes. This species was not related as common or abundant in Matasgordas, whose seed rain was nil, but its presence was highlighted in Reserva, whose seed rain under C. humilis accounted for 85-90% of the total seed rain. Even a few feces with dozen of R. ulmifolius seeds would certainly bias the results and the comparison between areas when the response variable “number of seeds” is considered. Would the spatial patterns be the same between the areas if R. ulmifolius is excluded from the analysis? If so, the conclusions presented by the authors should be revisited and adjusted to the bias introduced by this species.

I see these points do not invalidate the importance of C. humilis as perches and facilitative species in that habitat, but at least would provide more explanatory power for the distinct spatial patterns found between the two study sites. Besides that, I would recommend the authors to improve the English text, as some sentences are somewhat difficult to understand.

Bellow, I add some other specific points to the authors.

Page 4, lines 94-96: To question whether there are differences in the role of C. humilis as perches between the two areas presupposes some previous knowledge of the distributional pattern of this species between the areas. Although the authors provide a detailed description of the study areas in the proper session (pages 6 and 7) it should be enlightening to give a hint here on what triggered the idea that the plant role could be different between areas. Certainly, these two areas were not chosen at random.

Page 6, line 142: Delete the period after bourgaeana.

Page 7, lines 177-178: What was the total sampling effort for bird perching for the separate areas?

Page 9, lines 189-192: What do you mean by “palm interior”? Does it include the foliage surface in the interior and also the soil under the foliage? Was the open area of a similar surface associated with the palms bare soil? What were the criteria used to distinguish between bird-and-mammal dispersed seeds in these areas?

Page 14, lines 312-313: Since the number of feces and number of seeds are two interrelated response variables, what is the weight of the regurgitated seeds in the analysis? How much regurgitated seeds contributed to the total number of seeds sampled?

Page 16, line 375: Consider this writing: “Otherwise, in Reserva, the probability …”

Page 2, line 501: Insert “of” after “chances”.

Reviewer #2: Review MS:

Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L.

I have now carefully read the manuscript. I found the authors approach very interesting using SPPA to unravel the perching effect. Using this spatial analysis they evaluate several spatial patterns of “perching” effect and whether the seed arrival via frugivorous birds is related to the spatial distribution of the C. humilis in two disturbed scenarios. I think the manuscript could be interesting will be interesting for readers interested in restoration or ecological succession drivers.

I think the manuscript needs to improve the readability mostly in the methods and the results section (see comments below). I have concerns with the general work. On one hand, I think that it needs more information about the state of the selected plots. For instance, the main objective is to evaluate the perching effect based on the plants distribution, however, the authors did not show the spatial distribution of the individual plants, plants density, size of the plot, etc. that in my opinion has to be in the article. On the other hand, your main conclusions are based on some patterns found in one plot (male plants, isolation). This is my major concern because when you present the analysis of the other plot the main patterns did not applied to other ecological context. It seems that the results only applied under certain circumstances. I think this is a very common problem when studying the effects of perching which makes it very difficult to generalize the drivers of this process.

Abstract

L39- “dispersed seeds We detected” missed a point

Introduction

L97: Do exist some individuals of C. humilis that act as “hotspots” of dispersed seeds? Change for: Do any C. humilis individuals act as "hot spots" for seed dispersal?

Methods

L134-144. With this explanation it is unclear where did you work.

Reading some works made in the area it seems that Matasgordas has a higher plant density than Reserva. For instance, In the article by Fedriani and Delibes (2011) when the description of the Matasgordas site is made, it seems to have a higher density of individuals, same situation in the article by Jácome et al. 2016 where the spatial patterns of this species are studied where they also report higher number of individuals in the area. Thus, it would be interesting to specify that you do it “in a low density area in order to be comparable with Reserva.”

L163- Related with my previous comment. Although Reserva was protected earlier authors have to consider that there still traditional uses in the area, thus plants in the Reserva are submitted to a high herbivorous pressure due to the presence of horses, cattle and high density of cervids. This pressure has reflected in the lower density of individuals explained above.

Author response to Decision Letter 0

31 May 2022

Dear Dr. Karen Root,

We have now prepared a substantially revised version of our manuscript "Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L." (PONE-D-22-01669) submitted to Plos One. We would like to thank you and the reviewers for your thoughtful comments, and we are happy with the careful and constructive criticisms and helpful suggestions. In response to the comments, we have introduced the following three main changes:

1. As suggested by the editor and both reviewers, the manuscript has been carefully revised several times to improve the English grammar and flow of logic.

2. Following suggestion by reviewer #1, the role of birds as frugivorous and seed dispersers have been described in further detail. Also, some spatial analyses have been repeated excluding data from Rubus ulmifolius and the result are now provided in a new appendix.

3. As suggested by reviewer #2, we have conducted cluster analyses to estimate the distribution of C. humilis in both study plots. Also, we fitted a new GLM to estimate the effect of the interaction between palm height and palm area on seed arrival to C. humilis. Results of these new analyses are provided in the corresponding new appendices.

Please, find below an itemized list detailing how we have responded to each of the items in the reports. The comments are in black font, our response follows in blue font, and changed phrases in response to the comment are provided in blue font and between quotation marks and.

Thank you again for your kind assistance and the time devoted to our manuscript.

Sincerely,

1. Changes made to address editor comments:

Thank you for your suggestions. To address them, we made the following changes:

Lines 495-499 (previously 459-462): “Considering that our sampling period did not take place throughout the year and that an unknown fraction of the bird feces presents in target C. humilis individuals surely went unnoticed, the data obtained could be considered as a hint of how widespread the "perching” effect in both study plots. Therefore, the high presence of (frugivorous) bird feces and dispersed seeds in both study plots is remarkable.”.

Lines 501-504 (previously 465-467): “Nevertheless, we did not find seeds of the beneficiary species C. salviifolius, P. bourgaeana, Q. suber and S. genistoides, which are usually associated to C. humilis. Most of these plant species are seldom dispersed by birds”.

Lines 516-519 (previously 493-497): “However, by concentrating frugivorous activity to aggregated planted trees, seed dispersal could be limited [16, 55]. Therefore, our results supporting the role of isolated perches diverge from the most widespread tendency in ecological restoration of aggregating trees and shrubs during revegetation efforts [65]”.

Lines 523-526 (previously 508-511): “However, by concentrating frugivorous activity to aggregated planted trees, seed dispersal could be limited [16, 55]. Therefore, our results supporting the role of isolated perches diverge from the most widespread tendency in ecological restoration of aggregating trees and shrubs during revegetation efforts [65]”.

Lines 583-587 (previously 550-552): “Additionally, beyond the fact of bearing fleshy fruits, the own beneficiary species could be used as a perch and thus attract birds. Therefore, a similar reasoning explained earlier about how C. humilis height influences seed dispersal, could be applied for the revealed positive effect of height of beneficiary plants”.

Line 605-607: (previously 565-566): “In the last 30 years, restoration ecology has undergone considerable development thanks to the emerging new tools and techniques that facilitate the retrieval of biological properties of disturbed habitats [80]”.

Lines 635-638 (previously 594-596): “We prove for the first time its key role as natural perch, an ecological function that, though it is shared with some fleshy-fruited woody plants, is especially relevant in early stages of ecological succession when few pioneer species occur”.

Lines 288-289 (previously 268-269): “Finally, if km1. (r) ~ 1, indicates that the number of seeds is not affected by the distance to C. humilis individuals”.

Lines 531-533 (previously 502-503): “Besides, it seems reasonable to expect that birds select C. humilis located on the edge of the plot, since these individuals are closer to the Mediterranean scrubland and thus allow birds to move between habitats with a minimal consumption of energy”.

Previous lines 536-537: deleted.

Lines 598-600 (previously 559-561): “In summary, taller (and isolated) male C. humilis with a higher diversity of beneficiary species seemed to be the most suitable for attracting frugivorous birds and, therefore, received higher number of dispersed seeds”.

Regarding Reviewer #1’s concerns: we have improved our manuscript according to the comments received. We answered the questions related to the ecology of dispersers and did some new analyses without considering the Rubus’ seeds. We found that the results obtained when we excluded these seeds barely differed from the results obtained when those seed were included.

In respect of Reviewer #2’s comments, we have considerably improved the clarity and readability of the whole manuscript. We also added some information that Reviewer #2 considered important to clarify some aspects (C. humilis distribution, replicability, area of study, origin and identification of feces, etc.). We also run a new GLM including the interaction between C. humilis height (m) and area (m2) instead of the variable volume (m3), as suggested. The GLM obtained for both study plots (Matasgordas an Reserva) and for the three studied levels (presence of feces, presence of seeds and number of seeds) were pretty similar to the models obtained when the variable Volume was used. So, we provide the new model in the appendixes and kept the original one in the main text. We also carried out the analysis to study the distribution and level of aggregation of C. humilis. Our cluster analyses showed that Reserva has a greater percentage of isolated C. humilis, which is consistent with our results showing that birds prefer isolated C. humilis for perching in Reserva.

Line 63: “template” should be “temperate”

Thank you. Done.

Line 99: The use of the term “beneficiary” requires some type of description/definition or a reference source.

To address your comment have made the following change at Line 79-81: “Interestingly, in some cases, the same shrub species acting as perches also act as nurse plants, i.e. facilitating the emergence, growth and survival of other plant species, [23] which are designated as “beneficiary species”, promoting the natural (re)colonization [24, 25].”

Also, at Line 220-222, we now state: “Beneficiary species were woody plants that grow under dwarf palms and emerge from the top of their surface. These species often benefit from C. humilis due to microclimatic improvement and protection against herbivory [42].”

What characteristics define this group and is it context-dependent?

Thank you for such an interesting point. In Garrote et al (2019), some of us proved that there is a consistent and strong positive spatial association between C. humilis and several woody species. This result suggested that the interaction is constant rather than context dependent. Most recently (Garrote et al. 2022), however, we have showed through field experiments that the strength and even the sign of such interaction changes mostly with plant stages (seed survival, seedling emergence and survival), which would suggest context-dependency. However, the overall effect C. humilis on woody species was always either positive or neutral and whenever we detected neutral effects that result seemed associated to limited sample sizes. So, most compelling evidence indicate that, in overall, C. humilis exerts a consistent positive effect on woody species.

Garrote PJ, AR Castilla, JM Fedriani. 2019. The endemic Mediterranean dwarf palm boosts old-field recolonization: implications for restoration. Journal of Environmental Management 250: 109478.

Garrote PJ, A Castilla, JM Fedriani. 2022. Coping with changing plant-plant interactions in restoration ecology: effect of species, site, and individual variation. Applied Vegetation Sciences. DOI: 10.1111/avsc.12644

Line 232: Why 199 simulations? It seems like a rather arbitrary number. Is this based on some initial modeling or preliminary results?

The 199 simulations are the number recommended by Wiegand & Moloney (2013). They estimate the curve asymptotes for each spatial statistic (rank, P-value, etc.).

Wiegand, T., & Moloney, K. A. (2013). Handbook of spatial point-pattern analysis in ecology. CRC press.

Line 255: “that” should be “than”

Thank you. Done.

Journal Requirements:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

Reviewed and ensured.

We have added at Lines 131-132: “All permits necessary were granted by the National Park Service (ref. 2019/10) and the Junta de Andalucía (ref. 2019107300002261/IRM/MDCG/mes).”

Thank you. We have now specified JM Fedriani (who is affiliated at CSIC) as corresponding author in the Plos One manuscript submission platform. Also, in the manuscript both JM Fedriani and V Gonzalez-Garcia appear as corresponding authors.

https://figshare.com/articles/dataset/PerchigEffectDwarfPalm_xlsx/19642446

Sorry, we are not sure to fully understand your concern. Figure 1 and Figure 4 represent study areas sketch maps and study plots, respectively. They have been made by us specifically for this manuscript. To this aim, we used QGIS v3.18 software. So, we don’t see any copyright issue. However, we now provide the photo credit in Figure 2 and Figure 3 headings (Photo credit: Pedro J. Garrote) which was missing in the earlier manuscript version.

2. Changes made to address reviewer #1 comments:

Although there is a lot of consideration on the use of artificial perches in restoration, the role of natural perches deserves more investigation, especially in a poorly studied biome under this perspective, as is the case with Mediterranean Europe. In this regard, the authors provide an important dataset based on field observations and fine spatial analyses, which represents a great contribution to the restoration of that particular habitat.

Thank you very much for your suggestions and comments to improve our manuscript.

Lines 190-193: “Overall, nine bird species were recorded perching: Cisticola juncidis, Lanius senator, Phoenicurus ochruros, Phylloscopus collybita, Pica pica, Saxicola rubicola, Sturnus unicolor, Sylvia atricapilla and Sylvia melanocephala”.

All species but Cisticola, Lanius, Pica and Sturnus are reported by Herrera (1984) as frugivorous. However, Pica pica does include fleshy-fruits (Green et al. 2019) and acorns (Martínez-Baroja 2019) in their diet. Additionaly, genus Sturnus has been reported as fruit-eater too (Jordano 1987, Gonzalez-Varo et al. 2017), as well as genus Phoenicurus, Sylvia and Saxicola (Campo-Celada et al. 2022, Carnicer et al. 2009). Therefore, just two of our reported species (Cisticola juncidis and Lanius senator) would not participate directly in seed dispersal.

That is a good point even though during the fall and early winter (when our study was carried out) most of the recorded bird species (Table 1) shift their diet, at least partially, towards a frugivorous diet. To address your concern, we have added the following text in the discussion (Line 562-570): “However, we sampled during the seed dispersal season, time when some birds change their diet into a more fruit-based one. For instance, it has been reported that P. ochruros, S. atricapilla and S. malenocephala are able to quickly change their diet when fleshy fruits become available, while other species such as S. rubicola show a more gradual change to a frugivorous diet [67, 68]. Also, S. unicolor, P. ochruros, P. collybita, P. pica, and S. rubicola has been reported as fruit-eater, although in lesser quantities [69, 70, 71, 72, 73]. Therefore, although not all recorded bird species contribute equally to seed dispersal, fleshy fruits represent a considerable fraction of most of their diets during the seed dispersal season.”

Campo-Celada M, Jordano P, Benítez-López A, Gutiérrez-Expósito C, Rabadán-González J, Mendoza I. 2022. Assessing short and long-term variations in diversity, timing and body condition of frugivorous birds. Oikos, 2: e08387

Carnicer J, Jordano P, Melían CJ. 2009. The temporal dynamics of resource use by frugivorous birds: a network approach. Ecology, 90(7): 1958-1970.

Gonzalez-Varo JP, Carvalho CS, Arroyo JM, Jordano P. 2017. Unravelling seed dispersal through fragmented landscapes: Frugivore species operate unevenly as mobile links. Molecular Ecology, 26(16): 4309-4321.

Green AJ, Elmberg J, Lovas-Kiss A. 2019. Beyond Scatter-Hoarding and Frugivory: European Corvids as Overlooked Vectors for a Broad Range of Plants. Front. Ecol. Evol., 18.

Herrera CM. 1987. A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecological Monographs, 54(1): 1-23

Martínez-Baroja L, Pérez-Camacho L, Villar-Salvador P, Rebollo S, Quiles P, Gómez-Sánchez D, Molina-Morales M, Leverkus AB, Castro J, Rey-Benayas JM. 2019. Massive and effective acorn dispersal into agroforestry systems by an overlooked vector, the Eurasian magpie (Pica pica). Ecosphere, 10(12): e02989.

Thank you for your suggestion. We repeated our spatial analysis for the presence of seeds and for the number of seeds excluding Rubus’ seeds. The results obtained are pretty similar to the ones obtained initially when we included those seeds in the analysis. The results from such a new analysis are now included as Supporting Information (S2 Spatial seed analysis excluding Rubus’ seeds).

Besides that, I would recommend the authors to improve the English text, as some sentences are somewhat difficult to understand.

Thank you. We have carefully revised the manuscript several times to improve it language use and clarity. The revised manuscript has considerably improved in this respect.

Bellow, I add some other specific points to the authors.

Garrote et al. 2019 documented that Reserva presents higher density of shrubs than our study plot at Matasgordas. Such a difference in shrub cover led to a greater abundance of fleshy fruits in Reserva which likely makes this site more attractive to frugivorous birds.

Lines 137-138: “Study areas are different in terms of vegetation and human-use history [4, 38]”.

Lines 147-152: “Due to such past human activity, Matasgordas is now formed, mainly, by two habitats: (i) Scrubland dominated by P. lentiscus shrubs with some Q. suber and O. europaea var. sylvestris trees [4, 33] and (ii) an old-field, where our study plot was set, which woody vegetation is mainly composed by animal-dispersed native plants such as C. humilis, P. lentiscus, D. gnidium and P. bourgaeana, Asparagus aphyllus L., Halimium halimifolium (L.) Willk and Cistus salviifolius L. and scattered Q. suber and O. europaea var. sylvestris trees [4]”.

Lines 167-175: “Reserva (…) has been historically managed by human for agriculture, hunting, cattle grazing and tree felling, especially O. europaea var. sylvestris and Q. suber [41]. Reserva was protected earlier than Matasgordas, in 1964 and it has been recovering ever since, being recolonised by animal-dispersed plants such as A. aphyllus, C. humilis, Phillyrea angustifolia L. or R. ulmifolius [4]. This scrubland is dominated by H. halimifolium and Stauracanthus genistoides (Brot.) Samp. with scattered trees of Q. suber, O. europaea var. sylvestris and Pinus pinea [33]. The study plot at Reserva presents higher density of shrubs than the one at Matasgordas. Such a difference in shrub cover led to a greater abundance of fleshy fruits in Reserva, which likely makes this site more attractive to frugivorous birds [4].”.

Page 6, line 142: Delete the period after bourgaeana.

Thank you. Done.

Page 7, lines 177-178: What was the total sampling effort for bird perching for the separate areas?

Thank you for your comment. To address it, we have added the following text (Line 189-190) in the revised manuscript: “During the sampling, which lasted about 3h per day in Matasgordas and about 2h in Reserva, any observed bird perching on focal C. humilis individuals was recorded.”

Palm interior refers to the foliage surface since the soil under the palm was unreachable in most of the cases. Thus, we have replaced in the manuscript “palm interior” for “palm foliage surface”.

Yes, the open area associated to each palm was of similar surface (than the associated palm) and mostly in bare soil with scarce vegetation, mainly grasses. This open area was 3-4m from the associated C. humilis.

Lines 200-204: “Every target C. humilis was checked for bird feces and regurgitations by carefully checking the palm foliage surface. We also evaluated whether seeds arrive at open spaces without palms. To this aim, we checked for the presence of bird feces and regurgitations in an open area associated to each focal C. humilis. These areas were of similar surface and mostly located in bare soils with scarce vegetation (mainly grasses) and 3-4m from the associated C. humilis”.

What were the criteria used to distinguish between bird-and-mammal dispersed seeds in these areas?

Most sampled seeds were found within bird feces which are easily distinguishable from mammal feces based on size, shape, color and smell. For example, the uric acid in bird feces forms a conspicuous and white sticky paste that makes them easily to identify. Also, the diameter of feces of target birds (a few millimeters) was much smaller than for feces of local frugivorous mammal species (several centimeters).

Regurgitated seeds were just a small fraction of the total sample. Their number was too small to really contribute to the final analysis.

Page 16, line 375: Consider this writing: “Otherwise, in Reserva, the probability …”

Thank you. We have changed the sentence. Line 395-397 (previously line 375): “Results in Reserva substantially differed from results from Matasgordas. The probability of two C. humilis separated by distance r, having both seeds (p11(r) statistic), was similar to expected of random labelling for all spatial scales (Fig 6B).”

Page 2, line 501: Insert “of” after “chances”.

Thank you. Done.

3. Changes incorporated to address reviewer #2 comments:

Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L.

Thank you very much for your suggestions and comment to improve our manuscript.

I think the manuscript needs to improve the readability mostly in the methods and the results section (see comments below).

We have considerably improved the clarity and readability of the whole manuscript, including the methods and results sections.

I have concerns with the general work. On one hand, I think that it needs more information about the state of the selected plots. For instance, the main objective is to evaluate the perching effect based on the plants distribution, however, the authors did not show the spatial distribution of the individual plants, plants density, size of the plot, etc. that in my opinion has to be in the article.

Thank you for communicating this concern. Both Figure 1 and Figure 4 show the spatial distribution of the individual C. humilis. Following your suggestion, plant densities and plot sizes are now included in the Material and Methods section:

Line 136-137: “We selected two study plots 10 km apart called Matasgordas (area sampled: 13.9 ha) and Doñana Biological Reserve (area sampled: 21.4 ha)”.

Line 182-184: “The density of C. humilis plants in Matasgordas’ plot (7.78 individuals/ha) was pretty similar than in Reserva’ plot (8.41 individuals/ha).”.

On the other hand, your main conclusions are based on some patterns found in one plot (male plants, isolation). This is my major concern because when you present the analysis of the other plot the main patterns did not applied to other ecological context. It seems that the results only applied under certain circumstances. I think this is a very common problem when studying the effects of perching which makes it very difficult to generalize the drivers of this process.

We agree in that is very difficult to generalize the drivers of the perching effect. Differences in results between our study areas likely relate to the fact that they present a different state of ecological succession, an issue that is detailed in our Discussion and could be used by managers to decide, for example, whether particular areas are adequate to promote seed arrival using natural or artificial perches.

Abstract

L39- “dispersed seeds We detected” missed a point

Thank you. Done.

Introduction

L97: Do exist some individuals of C. humilis that act as “hotspots” of dispersed seeds? Change for: Do any C. humilis individuals act as "hot spots" for seed dispersal?

Changed for: Do particular C. humilis individuals act as "hot spots" of seed arrival, and if so, why? (Lines 99-100, previously Line 97).

Methods

L134-144. With this explanation it is unclear where did you work.

Thank you for your comment. The density for C. humilis is highly spatially heterogeneous both in Matasgordas and in Reserva areas. Thus, it is expectable that density changes depending on the specific location of the study plots in both areas. In our selected study plots, the density of C. humilis plants in Matasgordas (7.78 individuals/ha) was pretty similar to that in Reserva (8.41 individuals/ha) but, again, this could change if the plots were set in different specific locations. Ultimately, Matasgordas and Reserva were not too different in terms of palm density.

Our previous studies (Fedriani and Delibes 2011, Jácome et al. 2016) were carried out in Matasgordas and Reserva but their study plots were not the same that the pots of the present study; so, no wonder they reported other C. humilis densities. For instance, the study by Fedriani and Delibes (2011) was carried out in a patch of Mediterranean scrubland within Matasgordas area (where C. humilis density is certainly very high), whereas our present study was conducted in the old-field within Matasgordas area (where C. humilis density is much lower than in the scrubland).

To prevent possible misunderstandings in relation to this issue, we now consistently use throughout our manuscript the term study plot instead of study site.

As mentioned above, the densities of C. humilis in both Matasgordas (7.78 ind. ha-1) and Reserva (8.41 ind. ha-1) were not too different but, they could change depending on where the study plots are located.

Decision Letter 1

Karen Root

29 Jun 2022

PONE-D-22-01669R1Unmasking the perching effect of the pioneer Mediterranean palm Chamaerops humilis L.PLOS ONE

Dear Dr. Fedriani,

I appreciate the authors’ thoroughness and thoughtfulness in addressing the numerous comments and suggestions by the original reviewers. The paper examines an interesting restoration question about the role of perch plants for seed dispersal in disturbed environments. While it makes an important and timely contribution to our understanding of the effects of structure on seed dispersal the manuscript needed increased detail, clarity and improvement in the description of the study design, the analysis and the interpretation of the results. The revised version is much clearer and the results are much better supported. The new analyses are illuminating and provide important detail to the results. As the reviewers suggest there are still a few minor revisions that could further strengthen the paper and improve the readability. Please note, though, the reviewers for this version are not the original reviewers so they have provided a fresh perspective on the revised manuscript. As Reviewers 3 and 4 highlight, there are a number of places where some additional editing (e.g., improving the grammar) will improve the readability. As reviewer 3 suggests, it would also be help to refer to the sites in a consistent order to aid the reader in tracking the differences. Both reviewers have included detailed suggestions and clarifying language that should be considered throughout, which are included in the annotated versions. In addition, they have provided questions highlighting places where additional information or a rephrasing may be necessary. With these minor revisions, the paper should be well crafted to contribute to our understanding of the ecological implications of structure in restoration on seed dispersal.

Please submit your revised manuscript by Aug 13 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Karen Root, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #3: (No Response)

Reviewer #4: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Yes

Reviewer #4: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

Reviewer #4: I Don't Know

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4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

Reviewer #4: No

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: Yes

Reviewer #4: Yes

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6. Review Comments to the Author

Reviewer #3: A note that I was not a reviewer on the first round of the manuscript. I thought for the most part that the authors did a thorough job of responding to prior reviewers’ comments. Generally, the paper is clearly written and the analyses seemed sound. I did, however, make quite a few edits directly on the manuscript and think the manuscript needs another round of revisions. Here I just summarize a few key points.

1. Most of my comments are grammatical corrections (using either comments or in red text). I started doing a thorough edit but that is challenging with a pdf so only did so on the first couple of pages. The paper needs a thorough edit by somebody with a strong command of English grammar.

2. The authors refer to their two sites by the actual site names, but those site names are meaningless to the reader. Then the authors have to reminder the different characteristics of the sites. I suggest that the authors name the sites for the paper using what they think is the most distinguishing feature – e.g. early-successional and late-successional site.

3. The authors overstep their data in their restoration recommendations. They have data from only two sites and the results differ in the two sites, which is typical of restoration – results are often site-specific. So they have a limited ability to generalize. They also make recommendations in that section that don’t stem from the data presented. I strongly recommend that they combine their “recommendations” and “conclusions” section into one section and condense the restoration conclusions to 1 paragraph.

4. The authors frequently put modifying clauses in parentheses. In most cases, these should be part of the main sentence.

Please see the manuscript for additional comments and edits.

Reviewer #4: I made a series of minor suggestions/comments directly on the ms.

Regarding the availability of data, I found a vague statement that "all data are fully available without restriction", without any indication of how to access it.

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Reviewer #3: Yes: Karen Holl

Reviewer #4: No

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PLoS One. 2022 Aug 23;17(8):e0273311. doi: 10.1371/journal.pone.0273311.r004

Author response to Decision Letter 1

11 Jul 2022

RESPONSE TO EDITOR COMMENTS

-->Thank you very much for your positive comments. We have carefully followed comments by reviewer 3 and 4 to improve further the grammar and readability of our manuscript. We now refer to the study sites in a consistent order to aid the reader in tracking the differences. Also, we have included additional information or a rephrasing when necessary.

RESPONSE TO REVIEWER 3 COMMENTS

-->Thank you very much for your helpful comments.

-->We have addressed all grammatical corrections pointed by both reviewers. We have also revised again the whole manuscript ton improve its clarity and flow of logic.

-->The names of both study sites have been changes as suggested throughout the manuscript.

-->All these suggestions have been included in the revised manuscript.

4. The authors frequently put modifying clauses in parentheses. In most cases, these should be part of the main sentence.

-->We have included in the main sentences several clauses that used to be in parentheses.

Please see the manuscript for additional comments and edits.

-->We have addressed all comments and edits provided in the annotated manuscript. Below, I summarize the most relevant ones:

L472. How can height be negatively relate to number of seeds and size positively related?

-->There was a mistake in this sentence. Both height and area negatively relate to number of seeds, whereas volume was positively related. We have corrected these sentences.

L517-518. Or is it that the feces were more concentrated in single plants because there was only one?

-->Indeed, in late successional study plot (Reserva) there were more individuals that receive seeds (31) than in the early successional study plot (Matasgordas; 20).

RESPONSE TO REVIEWER 4 COMMENTS

Reviewer #4: I made a series of minor suggestions/comments directly on the ms.

-->Thank you for your comments and suggestions. All of them have been addressed in the revised manuscript.

Regarding the availability of data, I found a vague statement that "all data are fully available without restriction", without any indication of how to access it.

-->The data used for this study is fully available at:

https://figshare.com/articles/dataset/PerchigEffectDwarfPalm_xlsx/19642446

Attachment

Submitted filename: Response to Reviewers (2).docx

Click here for additional data file.^{(15.9KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0273311.r005

Decision Letter 2

Ignasi Torre

8 Aug 2022

Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L.

PONE-D-22-01669R2

Dear Dr. Fedriani,

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Additional Editor Comments (optional):

The article was reviewed again by rev. 3 and 4 and minor changes need to be done (some comments not addressed, grammatical and typographical errors).

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #3: All comments have been addressed

Reviewer #4: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #3: Yes

Reviewer #4: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

Reviewer #4: I Don't Know

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #3: Yes

Reviewer #4: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #3: No

Reviewer #4: Yes

**********

6. Review Comments to the Author

Reviewer #3: The authors have addressed all my substantive comments but there remain a number of typographical and grammatical errors. That said it would take extensive time for me to make those grammatical edits on a pdf version of the document and I don't have access to the Word version. I am not sure what type of resources PLOS One provide for English language proofing but the paper needs a careful edit for grammar.

Also, there should be a space between the numbers and units (e.g. 6 m not 6m) throughout. If the measurement is used as a an adjective then a dash is included (e.g. 6-m transect).

Reviewer #4: Two comments I raised before have not been addressed in this revision (pages 9 and 10 of the ms). I left them marked in the ms PDF file attached.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

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Reviewer #3: No

Reviewer #4: No

**********

PLoS One. doi: 10.1371/journal.pone.0273311.r006

Acceptance letter

Ignasi Torre

12 Aug 2022

PONE-D-22-01669R2

Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L.

Dear Dr. Fedriani:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Kind regards,

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on behalf of

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 File. Cluster analysis.

Technical details concerning the cluster analysis.

(DOCX)

Click here for additional data file.^{(12.3KB, docx)}

S2 File. Spatial analysis excluding Rubus’ seeds.

(DOCX)

Click here for additional data file.^{(12.3KB, docx)}

S1 Table. Summary of the results of the C. humilis distribution fitted with the Thomas cluster process.

(DOCX)

Click here for additional data file.^{(12.9KB, docx)}

S2 Table. GLM carried out to analyze the palm traits in the early-successional plot.

(DOCX)

Click here for additional data file.^{(15.7KB, docx)}

S3 Table. GLM carried out to analyze the palm traits in the late-successional plot.

(DOCX)

Click here for additional data file.^{(21KB, docx)}

S1 Fig

(DOCX)

Click here for additional data file.^{(131.7KB, docx)}

S2 Fig. Analysis of feces with seeds (excluding Rubus) in the late-successional study plot using mark connection functions as summary statistics.

(DOCX)

Click here for additional data file.^{(134.1KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(46.3KB, docx)}

Attachment

Submitted filename: PONE-D-22-01669_revision.pdf

Click here for additional data file.^{(3.5MB, pdf)}

Attachment

Submitted filename: PONE-D-22-01669_R1.pdf

Click here for additional data file.^{(3.4MB, pdf)}

Attachment

Submitted filename: Response to Reviewers (2).docx

Click here for additional data file.^{(15.9KB, docx)}

Data Availability Statement

All data files are fully available at: https://figshare.com/articles/dataset/PerchigEffectDwarfPalm_xlsx/19642446.

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PERMALINK

Unmasking the perching effect of the pioneer Mediterranean dwarf palm Chamaerops humilis L.

Víctor González-García

Pedro J Garrote

Jose M Fedriani

Roles

Abstract

Introduction

Material and methods

Study species

Study area and plots

Fig 1. The study plots.

Data collection

Fig 2. Birds using Chamaerops humilis as perches in Doñana National Park.

Table 1. Summary of collected data.

Fig 3. Examples of collected feces and identified dispersed seeds.

Spatial analyses

Aggregation of C. humilis used as perches within the overall pattern of C. humilis

Aggregation of C. humilis receiving dispersed seeds within the overall pattern of C. humili

Association of the number of dispersed seeds on C. humilis

Effect of palm traits

Results

Overall patterns

Fig 4. Distribution of C. humilis in the early-successional plot (upper) and the late-successional plot (lower) plots.

Spatial patterns

Fig 5. Analysis of C. humilis with feces in the two study plots (the early and late-successional plots) areas using mark connection functions as summary statistics.

Distribution of C. humilis receiving dispersed seeds within the overall pattern of C. humilis

Fig 6. Analysis of feces with seeds in the two study plots (the early and late-successional plots) using mark connection functions as summary statistics.

Distribution of the number of dispersed seeds across C. humilis

Fig 7. Mark correlation functions to evaluate a potential spatial structure in the number of dispersed seeds found on C. humilis in the early and late-successional study plots.

Effect of palm traits

Table 2. GLM carried out to analyze the palm traits in the early-successional plot.

Table 3. GLM carried out to analyze the palm traits the late-successional plot.

Discussion

Widespread perching effect by C. humilis

Spatial patterns of the perching effect

Palm trait’s influence on perching effect

Conclusions and implications for ecological restoration

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Karen Root

Roles

Author response to Decision Letter 0

Decision Letter 1

Karen Root

Roles

Author response to Decision Letter 1

Decision Letter 2

Ignasi Torre

Roles

Acceptance letter

Ignasi Torre

Roles

Associated Data

Supplementary Materials

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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