Biodiversity and biogeography of birds in Pacific Mexico along an isolation gradient from mainland Chamela via coastal Marias to oceanic Revillagigedo Islands

Following an isolation gradient in West-Mexico the avifauna of three study areas is investigated, on mainland reserve and two island groups. The avifaunas are described and analysed regarding species richness, environmental attributes, endemism, broader ecological niches, and brood status. The taxonomical composition is determined on different hierarchy levels. Most species records come from mainland Chamela (262), followed by the coastal Marias (191) and the oceanic Revillagigedos (148). Thereof 139 bird species breed in Chamela, 61 on Marias and only 29 on the Revillagigedos. In total, in the three study areas 364 species were recorded, which belong to 22 orders. On island groups generally less taxa per hierarchy level are present than on the mainland, especially on the remote Revillagigedos. Here, on average 1.7 species are found per genus, 2.2 genera per family, and 2.5 families per order. In the analysis of the taxonomical hierarchy relations to each other an isolation gradient is identified: from mainland Chamela via the coastal Marias to the oceanic Revillagigedos the degree of relatedness decreases on average. The results support the theoretical hypothesis that on islands closely related taxa tend to exclude each other and that one generalist tends to replace several specialists. Small ecological niches are often not occupied by specialist species on islands, but are used by generalists.


Introduction
A great proportion of the global biodiversity is hosted by islands, although these cover only about 2 % of the terrestrial surface of the earth.For example, 14 % of all terrestrial mammal species are found on them (Alcover et al., 1998), and 17 % of all bird species occur only on islands (WhittAker & Fernández-PAlAcios, 2007;comp. clements, 2000;dickinson, 2003).Because of their ability to fly, birds were able to reach nearly any island, to colonise it and evolve there.Therefore birds are highly suitable as study objects, especially to analyse the species richness on islands.
The geographical isolation of islands, mainly characterised by size and distance to other land masses, is considered as a main factor for species richness (mAcArthur & Wilson, 1967;cArlquist, 1974;WAlter, 1998;WhittAker & Fernández-PAlAcios, 2007;etc.).In course of time, in isolation great numbers of endemic bird species evolved on islands (e.g.moors, 1985;Johnson & stAttersField, 1990;GrAnt, 1998), and through adaptive radiation often increased the total species richness.As a result of their small distribution area and their specific life conditions, endemic island birds are highly sensitive against environmental changes (stAttersField & cAPPer, 2000).These changes are often caused directly or indirectly by man.Thus, in this sense many of these endemic species are indicators for the degree of nativity and/or change of an island ecosystem (comp. WeGe & lonG, 1995;stAttersField et al., 1998).
In the Mexican Pacific birds take a key position in the ecosystem of the oceanic Revillagigedo Islands (Jehl & PArkes, 1982).The latter belong to the few islands and places in general, which remained entirely untouched by mankind until the discovery of Spanish sailors in the 16 th century.The Polynesians in the West did not reach further than Easter Island and Hawaii.The American natives in the East stayed on the continent and some coastal islands.The late discovery is one reason for only limited anthropogenic shaping of the environment.In several regions of these islands native habitat lasted out (cAstellAnos & rodriGuez-es-trellA, 1993;mArtínez-Gómez & curry, 1998;mArtí nez-Gómez et al., 2001;BArBer et al., 2004) and few endemics yet have become extinct, contrasting the situation in central Polynesia (e.g. steAdmAn, 1989;1995).Thus, on these archipelagos it can be investigated how island bird populations develop, under natural-near as well as under man-made habitat conditions.
The avifauna of the Revillagigedo Islands is poorly known in general.A number of species accounts have been published (Anthony, 1898;BrAttstrom & hoWell, 1956;Jehl & PArkes, 1982;sAntAellA & sAdA, 1991;WehtJe et al., 1993;hoWell & WeBB, 1995;rodiGuez-estrellA et al., 1996); they are valuable but deal only with a limited part of the total spectrum of species.Then Fox quesAdA et al. (2004) gave a first overview based on more comprehensive field surveys.The coastal Marias island group is avifaunistically even less known (edWArds, 1998;hoWell & WeBB, 1995;sAntos del PrAdo GAscA et al., 2006;cAlderón hinoJosA et al., 2008); it is highly suitable for a biogeographical comparison with Revillagigedo because of its intermediate position just between the mainland and the high sea.Beginning in 2009 and continuing to 2010, own investigations have yielded a wealth of new avifaunal data from own field surveys and rarely known Mexican reports.
Based on the distribution pattern and selected study areas, it will be possible to investigate the effects upon island landbirds, specifically on their biogeographical characteristics, environments, and ecological characteristics in different degrees of isolation.Suitable as study areas are the oceanic Revillagigedo, the coastal Marias Islands, and the mainland nature reserve Chamela in the Mexican Pacific.This gradient of increasing isolation (longer distance to other landmasses/populations) represents a unique geographical constellation, and in the following is named "isolation gradient".
This survey aims to accomplish three principal goals.Firstly, it wants analyse the environmental attributes of all three study areas, and to make a comparison of all recorded species, breeders only, and endemics according to their spatial relations.Secondly, it wants to present an ecological approach to the avifauna of all three study areas.Species richness shall be given according to the three ecological groups of landbirds, freshwater birds and seabirds as well as according to their breeding status, basing on own field observations as well as data sources from references.Thirdly, the taxonomic composition of the avifauna shall be analysed in order to know which bird species, genera, families, and orders are present in the insular and mainland study areas, and in which proportion.Thus, generally we aim to identify the effect of isolation on bird species richness by investigating these three topics along a natural gradient including several endemic bird areas.

Study area and biogeographical background
For this work three different study areas are part of one terrestrial region and two marine regions.The terrestrial Chamela is located in a sub-humid, tropic area with a highly seasonal annual precipitation of 731 mm and an average temperature of 22.1 °C.The range of altitudes is from 10 m to 580 m including numerous Vertebrate Zoology n 62 (1) 2012   lands, respectively (e.g.mirAndA, 1960; villAreAl,  1972).(2003).Species in the lists were classified as breeders or non-breeders, and are additionally assigned to the single islands of the Marias and Revillagigedo groups.Endemic and extinct species were separately indicated.For comparison between the study areas, total numbers were summarised in order to calculate the ratios between recorded bird species, genera and family.Thus, ratios for hierarchical taxa relations were calculated by building average values from the total sums: R = ∑ S a + b + c / ∑ G A + B , where R is the ratio, S is the species ( a + b + c total number), and G the genera ( A + B total number) of a certain study area (comp.Table 3).

Results
In regard to bird numbers, the same tendency and a similar relation between mainland and island study areas is detected (Table 1).Bird species are more than eight times more abundant on the mainland, taking only breeding species into account even more than 16 times.Analysing the numbers of endemic bird taxa (on species and subspecies level), the situation appears to be different.In mainland Chamela no endemic taxon exists, as all breeding species also occur in other regions of Jalisco and/or Mexico.Contrarily, coastal Marias and oceanic Revillagigedo islands host 15 and 13 endemics, respectively.During the past centuries two endemics became extinct on Revillagigedo: the Socorro Elf Owl Micrathene whitneyi graysoni ridGeWAy, 1886 by human impact and the San Benedicto Rock Wren Salpinctes obsoletus exsul ridGWAy, 1903 by a natural eruption of a volcano.Taking the size of study areas into account, an endemism gradient is found plateaus and hills with steep hillsides.Most of the area has an altitude of not more than 150 m and is covered by over 1,100 different plant species (Estacion Chamela).
The group of costal Marias Islands has an average distance of about 100 km to the mainland and consists of four islands located in-line.The archipelago provides a surface area of more than 24,000 ha of which Isla Maria Madre covers more than the half.Not only this is the largest of the four islands but it also holds the highest elevation of this archipelago (640 m above sea level).Second largest is Maria Magdalena, followed by Maria Cleofas, and San Juanito.Climate conditions are similar to the mainland but there is less precipitation (564.2 mm) and a higher average temperature (24.9 °C) (cAlderon hinoJosA et al., 2008).The islands are covered by various types of vegetation composed by 387 plant species.On the different islands these plants are forming tropical deciduous and (tropical) sub-deciduous forests, with trees up to a height of 25 m.Furthermore shrubs, mangroves and cacti form other parts of the island vegetation.
Revillagigedo is an archipelago which closest part to the mainland is located about 550 km off the west coast of Mexico.This archipelago consists, in decreasing order of size, of Isla Socorro, Isla Clarion, San Benedicto, and Roca Partida.21 °C is the average annual temperature joined by a precipitation of 313.8 mm at sea-level, which creates a dry climate in this study area.The type of vegetation on these islands ranges from open grassland areas to small trees and shrubs with a maximum height of 3 meters (WehtJe et al., 1993).Recent volcanic activity influenced San Benedicto in the year 1953, and erased the population of the endemic Rock wren Salpinctes obsoletus exsul ridGWAy, 1903(BrAttstrom, 1990).
The single and small Isla Isabel (0.82 km 2 ) is located 30 km off the Mexican coast, about one third on the way to Marias Islands (sAntos del PrAdo GAscA et al., 2005).We have surveyed this island and its avifauna for ten days in 2010 (Appendix IV).However, because of the small area and the lack of other islands, it is not suitable for a direct comparison to the avifaunas of Marias and Revillagigedo archipelagos.
On the one hand the mainland study area, Chamela Reserve, covers a much smaller area than both island groups.This means that also the number of bird habitats is likely to be smaller.The lower maximum elevation of mainland Chamela of only 580 m a.s.l.represents another factor for a reduced bird (habitat) diversity compared to both archipelagos.On the other hand mainland Chamela shows a much better connectivity to other bird regions, being not isolated by water, and hosting a much higher number of plant species than both island groups.Mainland Chamela hosts more than 20 times more plant species per area than the is-via coastal Marias to oceanic Revillagigedo islands following the isolation gradient (Table 2).Amongst all recorded species, landbirds are very numerous in all three study areas (Fig. 1).However, their proportion on the entire avifauna decreases from mainland Chamela (71 %) via coastal Marias (68%) to oceanic Revillagigedo (45%).Species richness gradient is contrary in seabirds, as their proportion increases from mainland Chamela (21%) via coastal Marias (23%) to oceanic Revillagigedo (45%).Thus, in the Mexican Pacific only about half of the avifauna of oceanic islands is presented by landbirds, as seabird species become more numerous.The last group, freshwater bird species, are similarly rare in all three study areas: mainland Chamela (8%), Marias (9%), and Revillagigedo (10%).
The two contrary gradients for landbirds and seabirds are also present if taking only the breeding species into account.According to landbirds, 119 species regularly breed in mainland Chamela (representing 86% of this study area's total breeding avifauna), 54 on the coastal Marias (89%), and 16 on the oceanic Revillagigedo (55%).Thus, landbirds take an overwhelming part in the avifaunas of mainland and coastal islands, both in regard to breeders as well as non breeders.However, freshwater birds seem to be nonbreeding guests on the islands (except for one species, respectively) and mainly breed on the mainland.
The mean number of all recorded bird species per genus is not highly different between the three study areas (ranging from 1.53 to 1.72; comp.Table 3).However, analysing the higher taxonomic hierarchies, this gradient is found for four constellations: more species per family (5.6 < 4.7 < 3.7), more genera per family (3.6 < 2.8 < 2.2), more species per order (13.1 < 10.6 < 9.3), and more genera per order (8.6 < 6.4 < 5.4) are present towards the mainland.Only the relation of families per order is not clearly gradual, ranging from 2.28 to 2.5 (Table 3).Thus, in the taxonomical hierarchy relations a clear isolation from mainland Chamela via coastal Marias to oceanic Revillagigedo (0 < 0.06 < 0.08).Before the two extinctions, the relation was as high as one endemic taxon per 10 square kilometres.
A total of 364 bird species belonging to 22 orders have been recorded in the three study areas of Chamela, Marias, and Revillagigedo, of which 224 are considered to be regular breeders.Thus many of the recorded species are non-breeding visitors.The proportion of breeders on the overall avifauna decreases from mainland Chamela (53%) via coastal Marias (32%) to oceanic Revillagigedo (20%) islands (Fig. 1).Thus, relatively few birds manage to breed and establish a reproductive population on the islands, whereas about half of the recorded species do breed in the mainland reserve.Analyzing the total number of bird species separately for each of the three study areas, a decrease is detected regarding all recorded as well as the breeding species from mainland Chamela    Revillagigedo waters are rich in fish and other marine food sources (related overview in BrAttstrom, 1990), and offer protected resting and breeding grounds.Among the breeding avifauna, however, landbird species are more numerous than seabirds in all study areas.The relatively high number of landbird visitors on Marias and Revillagigedo Islands can be explained by the geographical position.Both archipelagos are placed far away from the mainland; however, they kind of are positioned in the western Pacific migration routes, especially for those birds following the Baja California Peninsula in autumn.Thus, the islands can be considered as important stop-over locations for migrant species (comp. BrAttstrom & hoWell, 1956;WehtJe et al., 1993).The heavy and abundant hurricanes hitting this region (average of three per season) represent another factor increasing the number of accidental guests and irregular vagrants on both island groups.Therefore further species records are to be expected in the future (comp.Jehl & PArkes, 1983).
Freshwater birds were recorded as visitors on the islands in remarkable numbers (although less than landbirds and seabirds), but nearly all species lack any breeding records.This may be due to the absence of lakes or lagoons, poor food sources in creeks, and high predation risk by raptors.Many of the island species have been recorded only few times, probably due to the low frequency and intensity of observation in these remote places.Contrarily, mainland Chamela reserve is much better known and monitored, as two professional ornithologists work here all year round (e.g.Arizmendi et al., 1990).
The relatively low ratio of Revillagigedo taxa belonging to the next higher taxonomic category (species per genus, genera per family, families per order) is suggested to be the result of isolation by distance, small area and limited habitats, as well as increased gradient is found: from mainland Chamela via the coastal Marias to the oceanic Revillagigedos the degree of relatedness of bird taxa overall decreases.

Discussion
The avifauna of the West-Mexican Pacific study areas is represented by a high number of bird species on the mainland, and relatively lower numbers on the oceanic islands, especially taking into account the breeders only (comp.also Jehl & PArkes, 1982;rodiGuez-estrellA et al., 1996).However, the results show that on the islands, especially on the remote Revillagigedos, isolation and difficulty of dispersal may not represent the prime reason for bird species scarcity.One may conclude that the critical point is the establishment of a permanent colonisation by immigrants, maybe in relation to limited habitat suitability.
Interestingly the majority of breeding species does only inhabit one of the two island groups, although dispersing to the other archipelago does not appear to be a critical factor: several specimens were seen on the other major island group but have not established a permanent population there.Thus the number of breeders is not limited by geographical isolation and low immigration rates, but also by ecological factors such as presence of suitable habitat, competition with resident species, and successful antagonistic strategies (hAhn et al., 2009).
Seabirds are as frequent as landbirds on oceanic Revillagigedo, but by no means in mainland Chamela.This is probably because most seabirds have large foraging, wandering and dispersal areas, and the competition for limited resources.It corresponds to the theoretical suggestions that closely related taxa tend to reduce each other and that one generalist of a taxonomic or ecological group tends to replace two or more specialists on islands; small niches are not occupied by a specialist species but covered by a generalist (lAck, 1969;diAmond, 1974;ABBott, 1980).However, all taxonomical ratio values are still higher than those of the South-eastern Pacific Juan Fernandez Islands off Chile (hAhn et al., 2009).The latter are less numerous, smaller in area size, and further away from any migration route.The resident landbird species pattern provides excellent support for these hypotheses.Most endemic landbird taxa originate from generalist species which are widely distributed on the (Mexican) mainland, not from specialists or continental restricted endemics.
For conservational concern, especially the endemic breeding birds of the islands are important.Distribution areas and number of habitats are generally very limited on these small archipelagos.The destruction of native habitat is particularly detrimental to the endemic taxa, since their habitat preferences are more selective than those of non-endemics (comp. rodiGuez-estrellA et al., 1996;hAhn et al., 2005hAhn et al., , 2011a, b), b).Most of the endemic species seem to be threatened today (restricted area and low abundance) and should be classified for conservation importance in the future (e.g.like done by WAlter 2004).Presently a third endemic taxon, the Socorro Dove Zenaida graysoni lAWrence, 1871 is close to extinction (only captive population maintained), and may speed up the recently high extinction rate on Revillagigedo.A reliable conservation ranking, including factors as habitat loss may prepare the basis for a more successful species management.Further threats seem to be the new invasive mammals on the islands (e.g.rodiGuez-estrellA et al., 1991;comp. also hAhn & römer, 2002).
Habitat destruction, mainly through man-made fires and introduced herbivores, is valued as the most serious concern for this critical situation.By destroying higher vegetation, herbivores are likely to have a negative effect on most scrubland and forest birds.Conservation management for the endemics must include the total eradication of introduced mammals.In spite of the present species inventories, very little is known about the endemic species.More detailed studies of the ecology of most endemics of Marias and Revillagigedo Islands are necessary.Such knowledge is urgently needed in order to develop conservation policies and regulations for the preservation of these unique bird assemblages.

For
being able to compare the study sites' avifaunal composition, occurring bird taxa are pooled in four lists representing mainland Chamela, Isabel Island, Marias Islands, and Revillagigedo Islands.Species lists are generated from a detailed, local literature survey (partly unpublished references; App.I-IV), and own additional fieldwork (App.I & IV).Own field data were collected in February and March of the years 2009 and 2010 in Chamela and Isabel Island.The reference sources, especially the grey Spanish reports, are indeed an important basis of the result chapter.Taxonomical classification in the attached species lists of recorded birds (appendices I-IV) is based on hoWell & WeBB (1995), and dickinson

Fig. 1 .
Fig. 1.Relative numbers of bird species recorded as breeders and non-breeding visitors in three study areas of the Mexican Pacific: mainland Chamela reserve, coastal Marias Islands, and oceanic Revillagigedo Islands.

Fig. 2
Fig. 2 -3.The Citreoline Trogon Trogon citreolus sumichrasti and the West-Mexican Chachalaca Ortalis poliocephala poliocephala are endemic to West-Mexico mainly restricted to the Pacific slope.Both are rather difficult to observe in the tropical deciduous forests of mainland Chamela reserve but are unmistakably identified and localised by their intensive calls.

Fig. 4
Fig. 4 -5.The Cinnamon Hummingbird Amazilia rutila rutila and the Streak-backed Oriole Icterus pustulatus microstictus were caught in the mainland Chamela reserve during the dry seasons in March 2009 and 2010.They also are distributed along the Pacific side of Mexico, their ranges reach further south to the evergreen tropical rainforests in Central America.

Table 1 .
Island attributes and bird species abundance in the Mexican Pacific study areas.Data originate from the sources of appendices I -III.

Table 2 .
Principal ecological types of bird species in the Mexican Pacific study areas.Data originate from the sources of appendices I -III.

Table 3 .
Hierarchical taxa relations of bird species in the Mexican Pacific study areas.Data originate from the sources of appendices I -III.