Conflicting selection on a plant seed size caused by native and alien seed dispersers.

It is well known that biological invasions modify the scenario for the native species triggering several consequences on local ecosystems functioning. Alien species, may cause abiotic shifts, competition for a source against native species, predation on local species, and mutualistic interactions as pollination or seed dispersion could be disrupt. This, in a long-term period lead to potential evolutionary consequences. Humans have been introducing until nowadays foreign species. The pine marten (Martes martes) among others was introduced 500 years ago in the Balearic Islands. This mammal feeds on Cneorum tricoccon fruits, ahead of, were dispersed only by endemic lizards (Podarcis lilfordi or Podarcis pityusensis). The Ecology Group has delved into how different pressure on the phenotipic fruit selection has been reflected on the seed size of C. tricoccon, comparing locations from islands and islets populated by lizards or pines marten.

C. tricoccon, is an evergreen shrub that can reach 1 m in height, although on average it is about 40 cm, has a restricted distribution to the western Mediterranean area, and whose main populations are currently found in the Balearic Islands. The only native seed dispersers of this plant species on this archipelago are two endemic lizards: P. lilfordi on islets around Mallorca and Menorca, not on the main islands and P. pityusensis in Eivissa, Formentera and islets around. Along the history, three species of carnivores have been introduced by humans which prey upon lizards: the least weasel (Mustela nivalis) by Romans, the common genet (Genetta genetta) by Muslims and the pine marten during Modern times. One of the reasons P. lilfordi is no longer on Mallorca and Menorca. Pine marten feed on animal preys but also on fruits, acting as effective seed disperser. In the study, we gathered data from 15 populations differing in the type of disperser: P. pityusensis was the only seed disperser in nine populations around Eivissa and Formentera, P. lilfordi in three islets close to Mallorca, and pine martens in the other three populations of Mallorca.

Geographical distribution of the study populations of Cneorum tricoccon (Rutaceae) in the Gymnesic islands (Northeast) and the Pityusic islands (Southwest) in the Balearic Islands. The unique seed dispersers for each population are pine martens (Martes martes) in Mallorca (TN: Tramuntana North, TC: Tramuntana Centre, TS: Tramuntana South), Podarcis lilfordi in three minor islands (DR:Dragonera, CA: Cabrera, CC: Conillera de Cabrera), and Podarcis pityusensis in Eivissa and Formentera islands, and surrounding islets (ES, S’Espartar; IB, Illa d’en Bosch; CE, Conillera d’Eivissa; TG, Tagomago; SC, Sa Canal; SE, S’Espalmador; SP, Espardell, BB, Cap de Barbaria; LM, La Mola). Latitude and longitude reference axes are also indicated.

Given the morphological differences in body size and gape width between pine martens and lizards, we might expect a different selection pattern on fruit size, which should translate into differences in the size of seeds dispersed. Native lizards consumed, limited by their gape width, select smaller fruits and thus dispersed smaller seeds, whereas the alien pine marten doesn’t present gape width constraint, to consume larger and more rewarding fruits, hence disperses larger seeds. In fact, pine martens eat simultaneously several fruits in a single feeding.

The study confirms that mean of seeds selected by pine martens, found in their droppings are larger than the mean of seeds of the plant, thus, is a positive selection. Instead, lizards show the opposite affair, choosing smaller seeds (from less rewarding fruit) than those available in their respective populations, showing a negative selection. This preference may be related to the trade-off between gape-width, pulp reward acquisition in the digestive track (perhaps, lizards have to defecate seeds rapidly to accelerate fruit processing and increase pulp assimilation, as happens with birds) but, also influenced by the predation risk. High risk predation scenarios, as smaller food pieces are handled more rapidly reducing the time spent exposed to predators. P. pityusensis (which shows much stronger anti-predatory strategies such as escape response) take so much smaller seeds than available, in comparison with P. lilfordi. One possible explanation for the differences between the two lizard species might be the different history of predation regime in each islet. Different spatial dispersion patterns are also crop up, due to pine marten has foraging ranges up to 1400m, transporting seeds to much longer distances than the native lizards whose territories are usually within the range of 100 m.

A previous study (Galetti et al. 2013) showed that the functional extinction of large-gape seed dispersers in the Brazilian Atlantic forest was associated with a consistent reduction in seed size of a keystone palm species. A recent phylogenetic analysis including more than 400 species across the Indo-Malayan archipelago has also revealed that average fruit size tracts the taxonomic and functional diversity of frugivores (Brodie 2017). We foresee that more evolutionary changes will be increasingly documented as mutualistic disruptions take place as a result of global change.

This study demonstrates that non-native frugivores can exert different selection pressures than native species and replace the ecological service provided by the extinct ones. The alien pine marten modified the selection regime on seed size of the native C. tricoccon compared to that exerted by native lizard species. 500 years ago, it might be enough time for that coexistence in Mallorca for them to promote phenotypic evolution on seed size. However, this result, is not leading negative consequences for native biodiversity and ecosystem functioning. Pine marten is acting as beneficial partner of C. tricoccon, and it can be functionally an adequate replacement.