This research aims to analyse the biodiversity of small birds (passerines) and its trends in a Western Mediterranean semi-arid wetland by means of captures for ringing during fourteen-years (1991-2014). The palustrine species outnumbered non-palustrine in individuals but not in species. The diversity of passerines is about two-fifth parts of the total diversity of birds of the wetland. Fourteen-palustrine species outweigh as dominants in number and biomass, belonging to the family Acrocephalidae or Reed warblers. The heavyweight of non-palustrine species is exerted by a Leaf warbler, the Common Chiffchaff Phylloscopus collybita. The biodiversity falls significantly over time with losses of 0.072 nats per year. Similar trends identified for the richness, which leaves losses of 1 species per year, ranging from 9 to 10 species gains and losses for the overall passerine’s assemblage. Diversity and richness correlate weakly and negatively with rainfall and positively with temperature, accounting from 15.1 to 20.4% of the variation in diversity of passerines, respectively. The loss of diversification of invertebrate preys due to global warming is considered a probable effect of the species decline.
Keywords: diversity, biomass, climatic change, passerines, trends, wetlands
Climatic change is already affecting many birds species in form of drifts of the departure or arrivals at their breeding areas,1,2 changing the populations dynamics,3 adaptations of the life cycle of migratory birds,4 changes in phenology,5 drifts in species distribution,6 changes in breeding outcomes,7 appearance of invaders and alien species which affect community patterns and population biology8,9 or increase or shorten the range of distribution of species6,10‒13 which provides a new global scenario for avian species distribution.14
In birds linked to wetlands, transformations in the habitat appear to be the main factor of the diversity loss.15‒17 Habitat disappearance in wetlands of SE Spain in the second half of past century produced losses of palustrine passerine species and decreases of about 10-80% of its effectives.18 This study intends to show up and to analyse the biodiversity of small birds (passerines) associated to wetlands in an internationally protected Spanish man-made swamp-wetland of 2500 Ha, during a temporal series of 14 years (1991-2004) trying to explore if the decline in its trends is due to the local climatic events as a proximate factor. In spite of time series deficit, the data may result very useful for future prospects, trying to establish plans for the management and conservation of reedbed passerine birds and their habitats.15,19
In view of the earlier, the following questions are established: 1) Which are the overall parameters measuring the biodiversity of the community of palustrine and non-palustrine passerines? 2) How is the trend of the biodiversity along years? 3) Which is the effect of climatic variations on the biodiversity at a local scale?.
Data for the present study arises from different sources: 1) captures of passerines get by means of ringing protocols implemented by the author during 1991-2004 in “El Hondo Natural Park”, an internationally man-made swamp-wetland protected as RAMSAR site of 2500 Ha of surface placed in SE Spain (38° 42’N 00° 31’W) and representative of wetlands of semiarid and fragmented landscapes in the Western Mediterranean. Diversity indexes of palustrine species and non-palustrine were measured separately by alpha’s Shannon’s Wienner Index expressed in nats20 and a comprehensive value representing the biodiversity of total passerines (Appendix 1). Maximum bird’s biodiversity of the wetland is calculated as Loge N (N=Number of all avian species listed for the Hondo Natural Park by).21 For the bird’s bioenergetics, it was considered the biomass of passerines as the product of the number of total individuals of each species by the weight of a sample of birds of each species taken during ringing protocols. During these ringing schemes, each species was measured and accurately classified by means of general Spanish checklists22 and European specific handbooks23 (Appendix 1). This is employed in other studies.24‒27 Most ringing visits were carried out in the morning, when the bird’s activity is higher28,29 but in some circumstances were conducted in the afternoon, so this might have influenced the probability of taking a less or more species in some years of research and some parameters of the community can have been thought influenced by wrong samples, however, dawn and evening sampling is found suitable for estimating the majority of reed passerines species.30 Rarefaction extrapolations were not done.31 Annual indexes of diversity and a number of species (richness) were plotted against years of study (1991-2004) in order to check the decrease of the species’ diversity along time (Figure 1). 2) Climatic variables are provided at a local scale (total amount of annual rainfall in mm and mean annual temperatures in °C) correlated with diversification in order to determine the effect of climatic change on the diversity’s trend. Non-parametric tests (Spearman correlations) and parametric (linear regressions) were achieved for these purposes using IBM SPSS v24 statistical package.32
Scientific name |
English name |
Number of individuals |
Individuals weigth (gr) Mean±SD (N) |
Palustrine status |
Biomass (gr) |
Hirundo rustica (Linnaeus, 1758) |
Barn Swallow |
5 |
18.6±1.7(5) |
NP |
93.0 |
Anthus pratensis (Linnaeus, 1758) |
Meadow Pipit |
4 |
16.5±0.7(2) |
P |
66.0 |
Troglodytes troglodytes (Linnaeus, 1718) |
Wren |
2 |
8.3±1.2(2) |
NP |
16.6 |
Erithacus rubecula (Linnaeus, 1758) |
Robin |
45 |
13.6±0.8(5) |
NP |
612.0 |
Luscinia megarhynchos (Brehm, 1831) |
Rufous Nightingale |
7 |
20.5±2.2(5) |
NP |
143.5 |
Luscina svecica (Linnaeus, 1758) |
Bluethorat |
134 |
16.4±1.6(5) |
P |
2197.6 |
Saxicola torquatus (Linnaeus, 1766) |
Common Stonechat |
24 |
13.1±0.9(5) |
NP |
314.4 |
Turdus merula (Linnaeus, 1758) |
Blackbird |
7 |
79.0±4.2(2) |
NP |
553.0 |
Turdus philomelos (Brehm, 1831) |
Song Thrush |
3 |
68.0±0.0(1) |
NP |
204.0 |
Cettia cetti (Temminck, 1820) |
Cetti's Warbler |
355 |
11.4±0.8(5) |
P |
4047.0 |
Cisticola juncidis (Rafinesque, 1810) |
Zitting Cisticola |
31 |
8.3±0.4(5) |
P |
257.3 |
Locustella luscionoides (Savi, 1834) |
Savi's Warbler |
20 |
15.7±1.5(5) |
P |
314.0 |
Locustella naevia (Boddaert, 1783) |
Grashopper Warbler |
1 |
16.9±0.2(2) |
P |
16.9 |
Acrocephalus melanopogon (Temminck, 1823) |
Moustached Warbler |
199 |
10.5±0.9(5) |
P |
2089.5 |
Acrocephalus paludicola (Vieillot, 1817) |
Aquatic Warber |
1 |
10.0±0.7(2) |
P |
10.0 |
Acrocephalus schoenobaenus (Linnaeus, 1758) |
Sedge Warbler |
13 |
11.1±0.6(5) |
P |
144.3 |
Acrocephalus scirpaceus (Hermann, 1804) |
Reed Warbler |
1832 |
10.4±0.4(5) |
P |
19052.8 |
Acrocephalu arundinaceus (Linnaeus, 1758) |
Great Reed Warbler |
227 |
29.2±2.2(5) |
P |
6628.4 |
Hippolais polyglotta (Vieillot, 1817) |
Melodious Warbler |
1 |
9.4±0.0(1) |
NP |
9.4 |
Sylvia undata (Boddaert, 1783) |
Dartford Warbler |
1 |
8.6±0.7(2) |
NP |
8.6 |
Sylvia cantillans (Pallas, 1764) |
Spectacled Warbler |
4 |
9.2±0.2(3) |
NP |
36.8 |
Sylvia melanocephala (Gmelin, 1788). |
Sardinian Warbler |
47 |
11.2±0.3(5) |
NP |
526.4 |
Sylvia borin (Boddaert, 1783) |
Garden Warbler |
2 |
20.6±1.8(2) |
NP |
41.2 |
Sylvia atricapilla (Linnaeus, 1758) |
Blackcap |
59 |
18.3±2.5(5) |
NP |
1079.7 |
Phylloscopus collybita (Vieillot, 1817) |
Common Chiffchaff |
1152 |
7.4±0.6(5) |
NP |
8524.8 |
Phylloscopus trochilus (Linnaeus, 1758) |
Willow Warbler |
17 |
9.1±0.5(5) |
NP |
154.7 |
Panurus biarmicus (Linnaeus, 1758) |
Bearded Tit |
198 |
13.2±0.6(5) |
P |
2613.6 |
Remiz pendulinus (Linnaeus, 1758) |
Penduline Tit |
33 |
9.2±0.6(5) |
P |
303.6 |
Parus major (Linnaeus, 1758) |
Great Tit |
4 |
17.6±0.6(3) |
NP |
70.4 |
Lanius meridionalis (Temminck, 1830) |
Southern Grey Shrike |
2 |
62.5±3.6(2) |
NP |
125.0 |
Passer domesticus (Linnaeus, 1758) |
Common Sparow |
9 |
28.1±1.2(3) |
NP |
252.9 |
Passer montanus (Linnaeus, 1758) |
Tree Sparrow |
1 |
17.3±0.0(1) |
NP |
17.3 |
Fringilla coelebs (Linnaeus, 1758) |
Common Chaffinch |
16 |
20.1±2.1(4) |
NP |
321.6 |
Serinus serinus (Linnaeus, 1758) |
European Serin |
7 |
10.8±0.5(4) |
NP |
75.6 |
Carduelis carduelis (Linnaeus, 1758) |
Goldfinch |
5 |
15.0±0.6(2) |
NP |
75.0 |
Carduelis chloris (Linnaeus, 1758) |
Greenfinch |
5 |
22.9±1.3(3) |
NP |
114.5 |
Emberiza schoeniclus (Linnaeus, 1758) |
Reed Bunting |
31 |
17.7±1.4(5) |
P |
548.7 |
Total samples |
|
417 |
|
|
|
Total Individuals |
|
4504 |
|
|
|
Total Passerine species |
|
37 |
|
|
|
Total palustrine species |
|
14 |
|
|
|
Total non palustrine species |
|
23 |
|
|
|
Number of palustrine's individuals |
|
2945 |
|
|
|
Number of non palustrine's individuals |
|
1559 |
|
|
|
Total Diversity (nats) |
|
1.919 |
|
|
|
Palustrine's diversity |
|
1.253 |
|
|
|
Non-Palustrine's diversity |
|
0.665 |
|
|
|
Total Biomass (gr) |
|
51660 |
|
|
|
Palustrine's biomass |
|
38290 |
|
|
|
Non-Palustrine's biomass |
|
13370 |
|
|
|
Appendix 1 Systematic List of Passerines in “El Hondo” Natural Park (Alicante, SE Spain)
The rainfall weakly tended to rise a long time and temperatures dropped in 1991-2004 period (Spearman r=0.20, p=0.493; temperatures: r=- 0.27; p=0363). By using long temporal dataset of 19 years (1991-2009) it is found a stronger significant increase of rainfall (Spearman r=0.50; p=0.029) and a weak increase of temperatures (r=0.29; p=0.224).
The entire number of passerine species was 37. The palustrine species (14) outnumbered non-palustrine in individuals but not in species (Appendix 1), so its diversity (1.26) is 66% of total passerines diversity and is about two fifth parts (37%) of the overall diversity of birds of the wetland (5.15) taking into account the full number of bird species of El Hondo Natural Park (N = 172).21 The rate of palustrine species is 38%. Only a few palustrine species refer to the family Acrocephalidae or Reed warblers which are Afrotropical passerines present largely in summer or migratory periods33,34 and exceeded in quantity and biomass as dominants (Appendix 1). The heavyweights of non-palustrine species (Appendix 1) was wielded by tiny Leaf warblers as Common Chiffchaff (Phylloscopus collybita).35 This is an opportunistic palustrine in winter in southern temperate areas of Western Palearctic36 but in breeding northern areas establish in mature lowland woodlands,37 so was not considered belonging palustrine in the community here analyzed (Appendix 1) . Both species suppose 70% of the absolute biomass of passerines (Appendix 1).
The biodiversity (Figure 2) falls significantly along time for non-passerines and total passerines while palustrine passerines showed a tendency to decrease. Similar trends are found for the richness of species (Figure 1). The rainfall correlates weakly and negatively with diversity and positively with temperature, so when rainfall increases, diversity reduces while it grows in parallel with temperatures. The percentage of variation in diversity of non-palustrines exerted by rainfall (r2=0.204, Figure 2) is the biggest determinant of change in diversity jointly with the variation in diversity of palustrine exerted by temperatures (r2=0.151, Figure 2). Linear regression among number of species on year resulted to be highly negatively significant and to be the determinant of the variation of species richness, giving losses of one species by year with a range between -10 and 9 of losses and gains in the total assemblage (Species=-1.413*Year+2838.484; F1,13=16.782, p<0.001, r2=0.583; Figure 1).
The results of this study essentially point out that the El Hondo Natural Park is a wetland relatively impoverished in biodiversity of passerines but valuable in reed-bed bird specialists or palustrine species, representative of the true assemblage. In general terms this is a poor passerine’s community with a global diversity index in the inner bound found for Shannon’s Index of 1.5 to 3.538 or from 1.8 to 5.3 for bird's communities39 and enters in the range of diversity (1.6-2.1) of Mediterranean reed-marsh communities.25,40‒44 Only two species, the Eurasian Reed Warbler (Acrocephalus scirpaceus) and the Common Chifffchaff (Phylloscopus collybita) suppose seven-parts of the total biomass of passerine community, illustrating the heavyweights of the assemblage.
It was found a negative effect of rainfall on the diversity, but a positive effect of temperatures on the fourteen years period (1991-2004). Longer temporal climatic datasets offer a rising of temperatures by the effect of climate change and this could have an effect in the diversity of palustrines by producing a fall in the non-palustrines diversity. In fact, long-temporal series of nineteen years (1991-2009) offer a non-significant increment of temperatures and significant increment of rainfall. The ecosystem gains and losses in a range of 9-10 species per year. This involves a great variation in passerine’s assemblage and harsh effects for its biodiversity. Other studies find that the number and proportion of long‐distance migrants decrease with increasing winter temperature, decreasing spring temperature, and increasing spring precipitation.45 Over a 13‐year period of warming temperatures, diversity indices increased while average community specialization decreased according to other studies.46 Habitat specialists and cold‐associated species showed consistently more negative effects of higher temperatures than habitat generalists and southerly distributed species associated with warm temperatures.47 The potential explanations of decline of species in El Hondo may be the loss of potential preys available, mostly Midges Chironomidae the most essential part of the diet of Common Chiffchaffs (Phylloscopus collybita) in El Hondo Natural Park48 and Beetles (Coleoptera) the gross for Acrocephalidae and Cettidae diet in wetlands of Western Iberia.49,50 In this form, climatic change can facilitate the extinction of invertebrates or modifications in its phenology51,52 which in turn can alter trophic interactions of the ecosystems.53,54
I thank Ministerio Medio Ambiente (Madrid) for permissions to use metallic-numbered rings and Comunidad de Riegos de Levante for giving me access to property and Generalitat Valencianafor permissions to ring in El Hondo Natural Park.
Author declares that there is no conflict of interest.
© . This is an open access article distributed under the terms of the, which permits unrestricted use, distribution, and build upon your work non-commercially.