Colony Foundation in an Oceanic Seabird

Abstract

Seabirds are colonial vertebrates that despite their great potential for long-range dispersal and colonization are reluctant to establish in novel locations, often recruiting close to their natal colony. The foundation of colonies is therefore a rare event in most seabird species and little is known about the colonization process in this group. The Cory's shearwater (Calonectris diomedea) is a pelagic seabird that has recently established three new colonies in Galicia (NE Atlantic) thus expanding its distribution range 500 km northwards. This study aimed to describe the establishment and early progress of the new Galician populations and to determine the genetic and morphometric characteristics of the individuals participating in these foundation events. Using 10 microsatellite loci, we tested the predictions supported by different seabird colonization models. Possibly three groups of non-breeders, adding up to around 200 birds, started visiting the Galician colonies in the mid 2000's and some of them eventually laid eggs and reproduced, thus establishing new breeding colonies. The Galician populations showed a high genetic diversity and a frequency of private alleles similar to or even higher than some of the large historical populations. Most individuals were assigned to several Atlantic populations and a few (if any) to Mediterranean colonies. Our study suggests that a large and admixed population is settling in Galicia, in agreement with predictions from island metapopulation models of colonization. Multiple source colonies imply that some birds colonizing Galicia were dispersing from very distant colonies (> 1500 km). Long-distance colonizations undertaken by relatively large and admixed groups of colonizers can help to explain the low levels of genetic structure over vast areas that are characteristic of most oceanic seabird species.

Fig 1. Colonization models proposed for seabirds in the literature: Mother-satellite, Stepping-stone and Island-metapopulation.

The diagrams show source (upper case) and newly founded (lower case) colonies with arrows indicating the flow of colonizers. The models support different predictions in terms of the genetic variability and private alleles (i.e. alleles that are not found in other sampled populations) of the founder populations as shown respectively in the lower section.

Fig 2. Location and development of the newly established colonies of Cory’s shearwaters in Galicia.

The bar charts show the number of apparently occupied burrows (AOB’s; open bars) and the number of burrows containing eggs (dark grey bars) and chicks (closed bars), in each of the newly established breeding colonies of Cory’s shearwater in Galicia (Coelleira, Sisargas and Cíes) during 2008–2014. The closed circles represent the size of the largest raft observed assembling near the colony during the main breeding season (May-August).

Fig 3. Private alleles.

Mean number of private alleles per locus (i.e. alleles that are not found in other sampled populations) as functions of standardized sample size (g). Private alleles were analyzed using: (a) individual Atlantic colonies and the Mediterranean group (Pantaleu, Aire and Habibas); (b) four combination of colonies, Galicia (Coelleira, Sisargas and Cíes), Atlantic (Azores, Desertas, Canarias and Berlengas), Selvagens and Mediterranean (see Fig 4 for rationale underlying this grouping); (c) private alleles of all pair combinations of the four major breeding areas. Private allelic richness for a pair combination estimates the number of distinct alleles private to a group of populations and found in all populations in the group, thus indicative of shared ancestry.

Fig 4. Population genetic structure of Cory’s shearwater.

(a) Factorial correspondence analysis performed on pairwise allele frequency differences using GENETIX v.4. (b) Population-level neighbour-joining tree based on F_ST across the 10 loci with per cent bootstrap support (10,000 replicates) shown at nodes. (c) Inferred ancestry (Q-matrix) of the two genetic clusters (red: Atlantic cluster; blue: Mediterranean cluster) for populations (upper panel) and individuals (lower panel) estimated by permutation from ten Structure analyses for individuals and populations, respectively, using Clumpp.

Fig 5. Assignment of Galician individuals to potential source populations.

(a-c) Discriminant Analysis of Principal Components (DAPC in adegenet) on Cory’s shearwater populations using three main reference areas (Core Atlantic, Selvagens and Mediterranean): (a) Scatter plot of individuals used as reference and groups as inertia ellipses according with two discriminant functions, representing 93% of variance (x-axis: first discriminant function [DF1], 66% of variance, y-axis: second discriminant function [DF2], 27% of variance); (b) Scatter plot of individuals from the three Galician colonies; (c) Number of individuals assigned to the main reference areas; (d) Heat plot of assignment probabilities of Cory’s shearwaters captured at the newly established Galician colonies. Each column represents an individual (50 females and 53 males) and colour the probability to be assigned to a reference population as estimated by GeneClass2. Probability was calculated independently for each population by Monte-Carlo resampling.

Fig 6. Morphometric comparison of Galician Cory´s shearwaters with those from populations elsewhere.

(a) Bivariate plot of wing length against tarsus length comparing the measurements of Cory’s shearwaters sampled in Galicia (Cíes, Sisargas and Coelleira) with the average values of Atlantic (red ovals) and Mediterranean (blue ovals) populations. Ovals are centered on the mean and the length of their axes is equal to one standard deviation. (b) Relationship between body size estimated as the first principal component (PC1) of a PCA analysis and the loadings in the first discriminant function (DF1) of the DAPC performed on microsatellite data (see Fig 5). Arrows indicate the two females assigned to the Mediterranean genetic cluster by the DAPC.

Fig 7. Individual tracks of the 11 Cory´s shearwaters that visited Galician waters to forage during the breeding season.

White stars correspond to the main breeding colonies where tracking studies have been conducted. Telemetry data was collected on the islands of (1) Corvo, (2) Graciosa, (3) Faial, (4) Santa Maria, (5) Berlenga, (6) Porto Santo, (7) Deserta, (8) Selvagem Grande, (9) Alegranza, (10) La Palma, (11) El Hierro, (12) Gran Canaria and, (13) Chafarinas. Black stars represent the three newly established breeding areas of (14) Coelleira, (15) Sisargas and (16) Cíes in Galicia. Four individuals from Berlenga (black), three from Porto Santo (blue) and two from Deserta (red) and one from Santa Maria (green) foraged off Galicia. See Table 3 for further details.