4 | Discussion
The heterozygous deficit and high levels of inbreeding with little or no
random mating deficit of heterozygotes, may be the result of the habitat
where the Chilean Palm lives and the existence of small and isolated
populations, which are maintained as a result of the form of
reproduction and seed dispersal.
The sclerophyllous forest inhabited by J. chilensis has been
highly exploited, leading to the species reduction over the years.
Currently, approximately only 121,284 specimens are left (or 2.5% of
the original population of the 19th century), being distributed among
highly fragmented populations (Bascuñán, 1889; González et al., 2017;
Rubinstein, 1969). These remaining populations are in an advanced stage
of aging, with little or no appearance of natural shoots, and under a
high anthropic impact due to the commercialization of their fruits and
sap (González et al., 2017). In addition, J. chilensispopulations present a clustered arrangement, which can both be related
to their inherent low long-distance capacity of seed dispersal as to
their relatively small effective sizes (González et al., 2017; Trénel et
al., 2008).
In the Pleistocene, seed dispersal was the product of endozoocoria by
the extinct megafauna species belonging to the following families:
Gomphotheriidae, Camelidae, Equidae, Notohippidae, Homalodotheriidae,
Toxodontidae, Astrapotheriidae, Macraucheniidae, Mylodontidae and
Megatheriidae (Carrasco, 2013; Gonzáles et al., 2017). Currently, the
seeds are dispersed in territories close to the mother plant as result
of gravity, floods and runoff. Although the main current dispersers are
humans who transfer the seeds to the different commercialization sites,
and the Octodont degus Molina and Spalacopus cyanus Molina
rodents that hoard the seeds, the recently introduced domestic species,
such as cattle and horses, also play an important effect, considering
that they remove, consume and regurgitate the seeds, but leaving them
susceptible to competition and desiccation (González et al., 2017;
Vander Wall & Longland, 2004). The frequency of rodent-seed interaction
is low (<25%) and transport usually occurs at short distances
(<6m) (Fleury et al., In Prep; Vander Wall & Longland, 2004),
indicating that rodent-dependent dispersion may be insufficient for
genetic exchange between existing palm groves, which leads to a lack of
gene flow and isolation between patches (González et al., 2017).
On the other hand, pollen can cover greater distance than seeds
(González et al., 2017; Kremer et al., 2012; Montúfar et al., 2011;
Sezen et al., 2005), but its movement is scarce once pollinators visit
mainly contiguous flowers of the same individual (González et al.,
2017). It has been described that in systems with restricted dispersal,
interruption of genetic connectivity occurs even in continuous
populations (Lowe et al., 2005; Nora et al., 2011; White et al., 1999).
All these factors may promote genetic isolation, lack of diversity and
inbreeding, leading to a reduced rate of populational change and
increased probability of extinction (Nora et al., 2011; Picó &
Quintana-Ascencio, 2005), as we observed here to Chilean palm. In
addition, the geographic distribution of palm groves is highly
fragmented, which implies that the populations are dissociated, forming
small independent groups, in which the degree of inbreeding increases as
a result of increased crosses between related individuals (Crawley,
1997; Picó & Quintana-Ascencio, 2005; Young &Clarke, 2000). When gene
flow is disrupted, populations can start a local differentiation process
that can lead to long-term speciation by genetic isolation (Herron &
Freeman, 2014).
Other limitations for J. chilensis regeneration are the
germination of seeds and establishment of the seedlings. Germination
occurs in a very long period, ranging from six months to four years,
occurring more frequently within approximately 18 months (González et
al., 2017). The growth stage of the seedlings is crucial for the
long-term survival of individuals (González, 2017) and can only be
achieved with the existence of a nurse plant understory of
sclerophyllous and/or spiny species, which provides the necessary
environment for their development until stipe’s formation (30-40 years)
(Del Fierro et al., 1998; González & Vita, 1987; González et al.,
2017). Valiente-Banuet et al. (2006) have shown that this nurse effect
prevented tertiary species from disappearing due to increased aridity in
the Quaternary. Palm trees (Arecaceae) that emerged in the Cretaceous
dispersed in the Early Tertiary Cenozoic and had significant extinction
rates in the Quaternary due to the rainforest’s retraction (Fleury et
al., 2015; Kissling et al., 2012). In Las Palmas, commune of Petorca,
previous studies have demonstrated that natural regeneration only occurs
in high-altitude areas with difficult access (Youlton et al., 2016).
Other studies on different taxa of the Arecaceae family have been
suggested that fragmentation considerably affects the permanence and
perpetuation of palm groves. In the south of the Brazilian Amazon,
forest fragmentation decreased Bactris Jacq . ex Scop. genus
(peach palm) palm reproduction due to inbreeding depression, possibly
leading to eventual extinction (Clement et al., 2009). For theAstrocaryum aculetassimum (Schott) Burret, an endemic species to
the Brazilian Atlantic Forest, it has been reported that the species
populations are highly affected by the loss of seed dispersers due to
fragmentation and hunting (Galetti et al. 2006). Also, for theAstrocaryum mexicanum Liebm. ex Mart. species inhabiting the Los
Tuxtlas (State of Veracruz / Mexico), has been shown that the abundance
of coleopterans and pollinating beetles varies according to the size of
the fragment (Aguirre & Dirzo, 2008). In Ecuador, the seedlings ofCeroxylon echinu latum Galeano and Attalea colenda (O.F.
Cook) Balslev & A.J. Hend. have failed to survive as a result of
deforestation (Anthelme et al., 2011; Borchsenius et al., 1998;
Montúfar, 2011). An extensive review of literature of palms from
Tropical America indicated that anthropic influences may cause changes
in the genetic structure, increased inbreeding and genetic drift in
fragmented populations (Montúfar, 2011). Similarly to this study, thePhoenix dactylifera L. populations occurring in natural oases in
Tunisia also presented HE values higher thanHO values, with low genetic structure and a long
period of isolation between sampled patches (Ben-Abdallah et al., 2020).
Some germination and establishment tests have been conducted forJ. chilensis seed (Cabello A., 1999; Infante L., 1989; Lewin L.,
2003; Saiz et al., 1989) as of the in the context of implementation of
the National Plan for the Conservation of Chilean Palm, carried out by
Chilean government (National Forest Corporation, CONAF) in 2005. This
Plan outlines a set of policy guidelines to restore/recover the species
populations throughout its distribution. Furthermore, since 2017
(Resolution 106/2017, CONAF) seed harvesters are officially prohibited
from harvesting in La Campana National Park, the largest palm grove
(~ 60% of existing palms). The J. chilensisharvest and management techniques, however, have not considered genetic
variability as a key factor in deciding which individuals or populations
should be restored or which territories should be protected. It is
essential that protective measures be based on multidisciplinary
analyses including genetic, ecological, reproductive and physiological
data. Currently, the Chilean palm is classified as Vulnerable (Benoit,
1989; Hechenleitner et al., 2005; IUCN / CMMC, 1994; Rodríguez et al.,
2005), and as in Danger of Extinction from the Chilean region of
Coquimbo (Squeo et al., 2001). We suggest that the current threat
classification consider too short time horizon, that might cause
underestimate the threats and underprotect the Chilean palm; and request
the re asses the J. chilensis extinction risk both the Danger of
Extinction and as a Natural Monument. Also, we underline that the
genetic variation must be considered in artificial propagation. This can
be specially useful for conserving species at risk, especially when
translocations for restoration, genetic rescue, or assisted gene flow
are fundamental aspects for the successful long-term population
(Flanagan et al. 2018) as the J. chilensis . The fact thatJ. chilensis is a monospecific, relict and endemic, with a patchy
distribution, no long-distance dispersal, no capacity for vegetative
propagation or sprouting large and recalcitrant seeds, and under severe
exploitation and anthropic impact may altogether argue in that sense.
Moreover, the high inbreeding and low populational genetic diversity
places the permanence of current and future populations at high risk due
to the lack of adaptation to environmental changes that allow them to
survive and evolve (Dawson et al., 2011; González et al., 2017; Jump et
al., 2009) especially in face of scenarios of climate changes and
negative anthropogenic effect.