Severe decline of threatened plovers at Bahía de Ceuta, Sinaloa, Mexico Clemens Küpper1,2*, Medardo Cruz-­‐López1,3, Wendy Rojas-­‐
Abreu4, Lydia Lozano-­‐Angulo1,5, M. Alejandro Serrano-­‐
Meneses1,3 1Ceuta Snowy Plover Project, Sinaloa, Mexico, www.chorlito.org 2Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford St, Cambridge, MA 02138, USA 3Centro Tlaxcala de Biología de la Conducta, Universidad Autónoma de Tlaxcala, Carretera Federal Tlaxcala-­‐
Puebla, Km. 1.5, Tlaxcala, C.P. 90002, Tlaxcala, Mexico 4Escuela de Biología, Benemérita Universidad Autónoma de Puebla, Blvd. Valsequillo y Av. San Claudio, Ciudad Universitaria, Col. Jardines de San Manuel C. P. 72570 5CISA, Tierras para la Conservación A.C., Agustina Ramírez 1222-­‐-­‐‐3, Col. Gabriel Leyva Solano, C.P. 80030, Culiacán, Sinaloa, Mexico *Present address: Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK Abstract Wetlands in Northwest Mexico provide critical habitat for both migrating and resident shorebirds. Bahía de Ceuta (23°54’N, 106°57’W) is a coastal wetland with high biodiversity located in Sinaloa, Mexico. We monitored the nest habitat selection and reproductive success of three ground nesting bird species that use Bahía de Ceuta for reproduction: Snowy Plover Charadrius nivosus, Wilson’s Plover C. wilsonia and Least Tern Sternula antillarum. We found 34 Snowy Plovers nests, eleven Wilson’s Plover nests and monitored 31 Least Tern nests over the breeding season. Snowy Plovers used similar open nest habitats largely located on mud flats or sites with small pebbles. Wilson’s Plover pairs preferred nesting sites that were covered by halophyte vegetation. This year Snowy Plovers shifted the breeding area further North in comparison with previous years. Wilson’s Plover and Snowy Plovers had similar nesting success (36% and 38% of the nests hatched). Nesting success was much lower for Least Terns. Only 7% of the monitored nests hatched. The 2012 breeding season ended as a complete failure for the local Snowy Plovers. Nest number declined by 52% in comparison with 2011 and not a single chick fledged. The long drought period followed by erratic flooding led to the observed failure this year but the lack of necessary conservation management actions compounded the situation. In the past Bahía de Ceuta hosted one of the largest Snowy Plover populations and an important Least Tern colony at the Pacific but if no appropriate conservation measures are taken the breeding site may vanish within a few years. 1 Introduction Wetlands often occur on the interphase between terrestrial and aquatic ecosystems. They are some of the most productive ecosystems that often harbour as much biodiversity in terms of species number as tropical rainforests. Wetlands are particularly important for flowering plants, molluscs, insects, fish, amphibians and birds. For example, it is estimated that approximately 10% of all bird species rely on wetlands as habitats during some stages of their life cycles (BirdLife International 2000). Wetlands also have important economic value providing water supplies, fish and crustaceans, flood defence, pollution dilution and recreation values (Long 2008, Verhoeven and Setter 2010). Despite the importance of wetlands and the services they provide, humans are increasingly threatening wetlands with the result that a large proportion has been lost or changed. Wetlands all over the world have been altered by draining and were converted into agricultural land or industrial and urban areas. It is estimated that at least 50 % of the world's wetlands have been lost (Verhoeven and Setter 2010). Northwest Mexico is particularly rich in wetlands. These wetlands are used by hundreds of thousands of migrating waterbirds with many shorebirds overwintering relying on coastal habitats (Engilis et al. 1998). Unfortunately, many wetlands in Northwest Mexico have been destroyed in the past. For example, the majority of the Mexican national shrimp industry is located in Sinaloa and about 60% of the shrimp farms that were built since the 1990s have converted natural salt marshes into highly intensified aquacultures. This development was triggered by favourable soil conditions and low property prices (Berlanga-­‐Robles et al. 2010) and gives a higher significance and importance to the conservation of the few remaining intact wetlands. Bahía de Ceuta is a coastal wetland located in Sinaloa (23°54’N, 106°57’W) that harbours an unusual high proportion of threatened biodiversity. It consists of a large lagoon of brackish water that is fed by a mix of fresh water (from irrigation) and sea water. The lagoon is surrounded by mangrove and dry forest vegetation. The adjacent beaches are annually used by threatened sea turtles that lay and burrow their eggs into the sand. Bahía de Ceuta is of regional importance for many overwintering waterbirds and it is additionally used for reproduction by resident marine and shorebirds (Küpper et al. 2009a). The importance of Bahía de Ceuta is acknowledged through national and international protection status as ‘Área Protegida’ (‘protected area’) which covers the breeding grounds of the sea turtles at the beaches and as RAMSAR site and Western Hemisphere Shorebird Reserve Network due to its relevance for migrating and resident shorebirds. Bahía de Ceuta is home for one of the largest populations of the threatened Snowy Plover Charadrius nivosus and Least Tern Sternula antillarum at the Pacific Coast of North America. Both species use the same breeding habitat and often breed in mixed colonies (Powell 2001). Snowy Plovers are small shorebirds endemic to the Americas (Page et al. 1995, Küpper et al. 2009b). They are breeding at sandy beaches and at alkaline salt lakes. Populations have been 2 in decline since the second half of the 20th century and Snowy Plovers that breed at the Pacific coast, in Florida and the Caribbean were declared endangered by US Fish and Wildlife Service at the end of the last millennium (US FWS 1993). Since 2010 the Snowy Plover has been also federally protected in Mexico and listed under the Norma Oficial Mexicana (NOM-­‐059-­‐SEMARNAT-­‐2010) as ‘threatened’. Snowy Plovers are one of the least numerous shorebirds and recent estimates suggest that most of the Mexican Snowy Plovers reside in the Pacific area but are in strong decline (Thomas et al. 2012). Similar to Snowy Plovers, Least Tern were once common across most of North America. However, their populations also declined steeply during the 20th century but after intensive conservation management Least Tern have rebounded (Powell 2001). Little is known about the abundance and taxonomic status of Least Tern in Mexico (Draheim et al. 2011). Early works suggest a small population of only 400 breeding pairs at the Northern Gulf of California (Palacios and Mellink 1996). However, during this census no survey was carried out in the states of Sinaloa and Nayarit and our own observations suggest that the colony at Bahía de Ceuta alone consists of 150-­‐250 breeding pairs (Cruz-­‐Lopéz et al. 2011, Küpper et al. unpublished). Since 2006 we have annually monitored the breeding success and behaviour of Snowy Plovers at Bahía de Ceuta. The high point of the population in terms of breeding activity and reproductive success was reached in 2007 when we recorded 140 nests and observed more than 100 families, of which 53 chicks fledged (Küpper et al. 2007). In 2008 we witnessed and abrupt decline of the population after which the population slowly rebounded (Lozano-­‐Angulo et al. 2008, Küpper et al. 2009a, Cruz-­‐Lopéz et al. 2011). Here we report reproductive success and breeding behaviour of Snowy Plovers, Least Tern and Wilson’s Plovers C. wilsonia during the 2012 breeding season. In contrast, to Snowy Plovers and Least Tern nothing is known about breeding abundance and population trajectories of Wilson’s Plovers in Mexico and we attempt to close this gap. First, we characterized the nest sites of both plover species and Least Terns. Second, we compared nesting success across the three species. Third, we identified recruits that hatched in Ceuta and returned for their first breeding attempts, and determined the proportion of breeders that were marked at Bahía de Ceuta in previous years. Fourth, we followed Snowy Plover families to determine parental care behaviour. Fifth, we determined reproductive success in Snowy Plovers families. Finally we will point out the problems Bahía de Ceuta is facing and recommend concrete conservation actions to tackle the open challenges. Methods Fieldwork was carried out between 29 April 2012 and 30 June 2012. Initial visits detected little breeding activity by any of the three species due to an ongoing severe drought that started earlier in the year. Therefore we only started daily fieldwork after 15 May when breeding finally picked up. We then searched exhaustively for Snowy Plover and Wilson’s Plover nests in the South Eastern part in all zones that were not flooded. 3 We used mobile hides for nest search and all identification of colour marked birds (Székely et al. 2008). Geographic positions of nests were taken using a handheld GPS unit. Eggs were measured and floated in fresh water to estimate clutch age. We assumed an incubation period of 25 days from clutch termination until hatching. Nests were checked every three to five days for predation or abandonment until a clutch age of 20 days. After this we checked the nests every other day until the chicks were pipping inside the eggs and thereafter daily. We searched for Snowy Plover and Wilson’s Plover nests exhaustively. To determine nesting success of terns we chose a sample of 32 active nests that roughly reflected the distribution of tern nests at the Bahía de Ceuta and monitored their survival until hatching as described before. To characterise the nest habitats of plover and tern nests we scored vegetation cover and soil type around the nest. At each nest the habitat for a 2 x 2 m square with the nest scrape in the middle was characterised to examine whether the different plover species had different habitat preferences. We measured different variables associated with vegetation and substrate in each square. For each variable the proportion of coverage was estimated. ‘Sand’ (grain size < 0.5 cm), ‘Pebble’ (0.5 – 2 cm), ‘Gravel’ (2 – 5 cm) and ‘Stone’ (> 5 cm) were variables to characterise the substrate. ‘Vegetation cover on the ground’ and ‘Vegetation cover at 10 cm’ was chosen to describe vegetation density and cover. We then used a linear discriminant analysis to test whether nests of both plover species could be separated according to habitat characteristics. We compared the reproductive success of both breeding plover species and terns by examining nest fates and comparing daily and total survival probabilities. Since terns are largely monogamous and the monitored nests were chosen within a two-­‐week period we are confident that each nest presented the breeding attempt of a different pair. We calculated daily survival probabilities and total survival probabilities according to nest exposure using the method suggested by Mayfield (1975). We captured adult plovers on nests. Parents were trapped on their nests using funnel traps after the clutch had been incubated for at least five days. We refrained from capturing on freshly laid clutches since plovers can be very sensible to disturbance at an early stage of incubation (Székely et al. 2008). Snowy Plover adults were marked with a metal ring and an individual combination of three colour rings, whilst all Wilson’s Plovers were marked with a single metal ring only. On the day of hatching we measured tarsus length and body weight of the chicks. Snowy plover chicks were marked with a single colour and metal ring. Chicks from the same family were assigned different colours to determine individual’s fates. A small blood sample (25µl of chicks and 50µl of adults) was taken from all captured individuals for subsequent genetic analyses. Snowy Plover families were monitored for survival until the chicks had reached fledging (about 25 days after hatching) or all chicks had died. Families were identified according to the marked parents who attended the broods. When a family was encountered we noted our position and the heading of the family 4 using a GPS handheld device (Garmin) and estimated the distance between the observer and the family to calculate the family position subsequently. We also recorded the attending parent and the number of chicks. A typical encounter was terminated when we resighted all chicks and the attending parent(s). If a family member was not found we continued to search for the missing member by scanning the vicinity of the family for at least 15 min before we concluded whether the family member was present or not. Parental desertion was concluded if a parent was absent at two or more consecutive encounters or found to be re-­‐mated. We took the mean between the last observation the parent had attended the family and the first observation without the attending parent as the date of desertion. Death of chicks was concluded if the last attending parent(s) were alone for at least 15 min, and they did not display defence behaviour. 5 Results W
N W
W
N
S
N
S
W
N
S
S
0
N
S N
S
W
S
S
-2
LD2 (Substrate)
2
4
Nest habitats of Snowy Plovers and Wilson’s Plovers Nests habitats of the three species differed in substrate and vegetation characteristics. Wilson’s Plover nests were largely located in halophyte vegetation on fine sandy dry mud substrate. Least Tern nests were found in the open with sandy substrate or on pebbles with no vegetation. About half (55%) of the tern nests had the same habitat and were located on dry mudflat without any vegetation. Most (80%) Snowy Plover nests were also found in this habitat and were located on dry mud flats (sandy substrate) without vegetation. However, a few Snowy Plovers also nested in vegetation or on pebbles overlapping with tern and Wilson’s Plover nest habitats (Figure 1). S S
W
W
W
W
S
S
S
SS
-6
-4
W
-2
0
2
4
6
8
LD1 (Vegetation)
Figure 1. Results of the least discriminant analyses to separate nest habitats of three plover and tern species at Bahía de Ceuta. ‘N’ refers to Snowy Plover nests, ‘W’ to Wilson’s Plover nests and ‘S’ to Least Tern nests. Symbol size indicates the number of nests with the same habitat characteristics. The Least Discriminant analyses suggested LD1 with predominant characteristics of vegetation (size and cover) as the best separator of the three species (LD1, Proportion of trace: 0.86) whereas LD2 with predominant substrate characteristics were less diagnostic (LD2, Proportion of trace 0.14). Nest fates Daily survival rates were 0.975 for Snowy Plover nests, 0.974 for Wilson’s Plover nests and 0.956 for Least Tern nests. Assuming an average incubation time of 25 days (plus six days egg laying period) for three-­‐egg clutches of both plover species and 22 (plus four days) for the two-­‐egg Least Tern clutches total survival 6 probabilities were 0.46 and 0.44 for Snowy and Wilson’s Plover clutches and 0.31 for Least Tern clutches. Nest fates and causes of failures differed significantly between species when nests with unknown fates were excluded (Figures 2–4, χ2-­‐test, χ2 = 16.5, df = 6, p = 0.001). Snowy Plover and Wilson’s Plover had similar nesting success (38% and 36%, respectively) as already suggested by similar survival rates. However, Snowy Plover nests were most vulnerable to flooding (29%) although they had the lowest predation rate of all three species (21%, Figure 2) whereas Wilson’s Plover nests were not affected by flooding but suffered from high predation (55%, Figure 3). In total, nesting success was lowest in the sample of Least Tern nests (7%) due to a combination of high predation (45%), flooding (16%) and high nest abandonment (16%, Figure 4). Snowy Plover (34) 6% Hatched 6% 38% 29% Predated Flooded Abandoned 21% Unknown Figure 2. Nest fates of all found Snowy Plover nests at Bahía de Ceuta in 2012. Number of nests is given in parentheses. Wilson's Plover (11) 0% 9% 36% Hatched Predated Unknown 55% Figure 3. Nest fates of all found Wilson’s Plover nests at Bahía de Ceuta in 2012. Number of nests is given in parentheses. 7 Least Tern (31) 16% 7% Hatched 16% 45% 16% Predated Flooded Abandoned Unknown Figure 4. Nest fates of a sample of Least Tern nests at Bahía de Ceuta in 2012 chosen randomly representatively from their breeding areas. Number of nests is given in parentheses. Thirty-­‐one chicks hatched from 13 Snowy Plover nests, eleven chicks hatched from four Wilson’s Plover nests and four chicks hatched from the two successful tern nests. Snowy Plover nesting Breeding was much reduced in comparison to previous years. We only found 34 nests, representing a decline by 52% to the previous year. Because of a large drought in Northwest Mexico, breeding grounds at Bahía de Ceuta had very low water levels by March, and plovers started breeding only in late April, with incubation at the first nest found starting only on 30 April. Breeding quickly picked up and 70% of the total nests were laid during a two-­‐week period between 4 May and 18 May (Figure 5). The breeding season was short in comparison with previous years and was concluded about one month earlier than usual, with the last nest being laid on 9 June. 8 Number of Snowy Plover nests 4 3 2 1 0 Laying date Figure 6. Laying date of 34 Snowy Plover nests found at Bahía de Ceuta in 2012. The Snowy Plovers also used areas further north nesting closer to the lagoon this year than previously. In the lagoon area, water was still available during the drought. We found 21 (62%) of the nests north of the salt works, the main nesting area of previous years. However, the spring tides coupled with strong Northern winds carried a lot of water south flooding all active plover nests outside the salt works and whereas the active nests in the salt works, south of the bordering dykes remained unharmed. Snowy Plover captures In total we captured 57 adult (25 female and 32 male) Snowy Plovers. Seventeen adults (eight males and nine females) were marked newly. Twelve further adults (six males and six females) were new recruits that had hatched in Ceuta between 2009 and 2011 and were marked as chicks already. In total 22 (39%) of the recorded breeding adults (eight females and 14 males) originated from Ceuta and have hatched in Ceuta between 2006 and 2011. Twenty-­‐seven of the 31 hatchlings were captured and marked whereas the remaining four chicks had already left the nest and presumably died before we were able to capture them. Snowy Plover broods We sighted twelve of the 13 Snowy Plover families tending chicks at Bahía de Ceuta after the chicks had hatched. Three families were deserted by the female parent after on average 2.8 days (range 0.5 – 4.5 days) after hatching. In the other nine families both parents attended the chicks on the last day of re-­‐
sighting. None of the deserting females started a new clutch at Bahía de Ceuta. No Snowy Plover chick survived until fledging because of adverse conditions this year. The chick that survived longest reached an age of ten days. 9 Discussion The 2012 breeding season was a complete failure for the threatened Snowy Plovers at Bahía de Ceuta. Because of constantly deteriorating conditions over the last years and bad weather including a prolonged drought, followed by an unexpectedly early and rapid flooding (Figure 7), not a single Snowy Plover chick fledged at Bahía de Ceuta this year. By contrast, in previous years we recorded 18 – 53 fledglings per year (Cruz-­‐Lopez 2011, Küpper et al. 2009a). Figure 7. Contrasting conditions at Bahía de Ceuta during the breeding season in 2012. Left: The severe drought lead to low water levels in the beginning of the season with the main breeding site (the abandoned salt work) completely drying out by early May. Right: A mobile bird hide flooded over night. Sudden strong tides that pushed tidal water into dry parts of the breeding area surprised ground breeding shorebirds, terns and monitoring researchers alike. It is not clear whether this year was an exceptional outlier or rather the continuation of the strong population decline that we have already noted since 2008. Worryingly, we noted that less than half of the population from 2012 were present to breed this year. On top of this, a large proportion of nests was flooded and all chicks died. Therefore hatching success for Snowy Plovers was much lower than in previous years (Cruz-­‐Lopéz 2011). The breeding season was also much shorter than any season we have monitored since 2006. Initially the Snowy Plovers adjusted to the dry conditions by postponing the onset of breeding. However, when conditions did not improve by late April breeding finally started. A large part of the population stated to breed in the Northern part of the Bahía where water was still accessible. Unfortunately, a sudden change of weather and the incoming spring tides flooded many nests of the lagoon breeders whereas the few chicks that had hatched presumably drowned. In contrast none of nests of the of the plovers that laid their nests in the salt works was flooded and most of these nests hatched although their chicks later died from starvation because of the lack of water in this area. Interestingly, the Wilson’s Plovers and the majority of terns did not shift their nest locations. We found most nests as previously in the abandoned salt works. Tern chicks are fed shrimps or fish by the parents whereas plover chicks are precocial and have to find their food themselves. Tern parents can cover the distance to the water and fly over obstacles such as the mangrove forest that is impenetrable for Snowy Plover families with small chicks. The nests in the abandoned salt works were also safer from flooding. Snowy Plovers rely on open habitat with no or low vegetation cover. This is different to Wilson’s Plovers 10 families which we often observed in denser vegetation with more humid soil conditions. However, since we did not monitor Wilson’s Plover families it is unclear whether their chicks survived better than Snowy Plover chicks. Figure 8. Freshly hatched Snowy Plover chicks (left) and Wilson’s Plover chicks (right) at Bahía de Ceuta. All three ground nesting species overlapped with their choice of habitat. However, Wilson’s Plovers nests were found mainly in areas, which were at least partly covered by vegetation whereas Least Terns and Snowy Plover nests were found in areas with little or no vegetation such as dry mudflats. Despite the similarity of nest sites predation rates differed between species. This is particularly interesting for the comparison of Snowy Plovers and Least Terns that shared many nest site characteristics and were often breeding in close proximity of each other. The higher predation rate and lower survival rates of Least Tern nests could be caused by differences in nest/egg camouflage or behaviour. Least Terns are much more conspicuous than plovers at their nest and predators might use these cues to locate their nests. Wilson’s Plovers and Snowy Plovers nests had similar survival rates despite the fact that nearly two out of five Snowy Plover nests but not a single Wilson’s Plover nest were flooded. This is because a larger proportion of Wilson’s Plover nests were predated. Recommendations for conservation management Bahía de Ceuta can be an ideal place for rare birds and could be a popular visiting place for tourists interested in the natural treasures of Northwest Mexico. Sustainable eco-­‐tourism could provide an important economic resource for local communities and landowners. However, currently the future prospects for the are look rather bleak since conservation progress has been halted and no new management action that are urgently needed have been implemented over the last ten years. Our results particularly highlight severe problems for the ground nesting birds at Bahía de Ceuta. If no further conservation actions are started the populations of threatened plovers and terns may disappear within a few years. § One of the principal problems is the deterioration of habitat. The dyke system is unable to hold off the water during the nesting season whilst during the brood season the water evaporates too fast. We recommend repairing and restoring the existing dam and canal structure of the salt works as well as adding a number of shallow ponds where water can 11 accumulate and act as a reservoir during the dry season. These ponds will then provide a stable food source for shorebird and tern families across the breeding season. §
The destruction of the surrounding dry forest and mangrove habitat is still continuing. More efficient policing is needed to stop illegal logging and construction activities. We noted that the disturbance through humans and feral cats and dogs, and pollution by illegal trash dumping in the area is increasing annually despite the clear and visible sign posting placed by us and governmental conservation agency CONAP. More environmental education programmes may be needed to increase sensitivity of locals and visitors alike. §
The concession holders of the salt work area, researchers and conservationists should work together on conservation management. Better communication and regular meetings are needed to plan and finally implement conservation actions. Without better management the habitat will be unsuitable for ground nesting birds within a few years. §
The monitoring of plovers and terns should be continued. Better data are needed to evaluate the effect of climate change on the local breeding populations of plovers and terns that represent a substantial proportion of the global population of these threatened species. Acknowledgments Our work was funded by CONACyT grant (Ciencia Básica 2010-­‐01, project number 157570) to MASM and a Blake Nuttall grant to CK. Permissions for fieldwork were given by SEMARNAT and CONABIO to CISA AC. References Berlanga-­‐Robles, C.A., Ruiz-­‐Luna, A., Bocco, G. and Vekerdy, Z. (2011) Spatial analysis of the impact of shrimp culture on the coastal wetlands on the Northern coast of Sinaloa, Mexico. Ocean & Coastal Management 54, 535-­‐543. Birdlife International (2000) Threatened birds of the world, Lynx Edicions and BirdLife International, Barcelona and Cambridge, UK. Cruz-­‐López, M., Beamonte-­‐Barrientos, R., Rojas-­‐Abreu, W., Sanchez-­‐Velazquez, O., Alvarado-­‐
Alapizco, L.F. and Küpper, C. (2011) Ecology and reproductive success of snowy plover Charadrius nivosus and least tern Sternula antillarum at Bahía de Ceuta, Sinaloa, Mexico, p. 12, Universidad Autónoma de Tlaxcala. Draheim, H.M., Miller, M.P., Baird, P. and Haig, S.M. (2010) Subspecific status and population genetic structure of least terns (Sternula antillarum) inferred by mitochondrial DNA control-­‐region sequences and microsatellite DNA. Auk 127, 807-­‐819. Engilis, A., Oring, L.W., Carrera, E., Nelson, J.W. and Lopez, A.M. (1998) Shorebird surveys in Ensenada Pabellones and Bahia Santa Maria, Sinaloa, Mexico: Critical winter habitats for Pacific flyway shorebirds. Wilson Bulletin 110, 332-­‐341. Küpper, C., Cruz-­‐López, M., Alvarado-­‐Castro, K.L., Fonseca-­‐Perra, J. and Bucio-­‐Pacheco, M. (2009a) Breeding ecology of Charadrius plovers at Ceuta Bay, Mexico, p. 14, University of Bath. Küpper, C., Lozano-­‐Angulo, L., Cruz-­‐López, M. and Bucio-­‐Pacheco, M. (2007) Reproductive success and parental care of snowy plover Charadrius alexandrinus nivosus in Ceuta, Mexico, p. 14, University of Bath. 12 Küpper, C., Augustin, J., Kosztolányi, A., Figuerola, J., Burke, T. and Székely, T. (2009b) Kentish versus Snowy Plover: Phenotypic and genetic analyses of Charadrius alexandrinus reveal divergence of Eurasian and American subspecies. Auk 126, 839−852. Long, P. (2008) Ecological and life-­‐history basis of wetland bird conservation: phylogenetic and spatial analyses, PhD Thesis, University of Bath, Bath. Lozano-­‐Angulo, L., Cruz-­‐López, M., Argüelles-­‐Tico, A., Bucio-­‐Pacheco, M. and Küpper, C. (2008) Reproductive success and parental care of snowy plovers Charadrius alexandrinus nivosus in Ceuta, México, p. 11, University of Bath. Mayfield, H.F. (1975) Suggestions for calculating nest success. Wilson Bulletin 87, 456-­‐466. Page, G.W., Warriner, J.S., Warriner, J.C. and Paton, P.W.C. (1995) The Birds of North America, No. 154. Poole, A. and Gill, F. (eds), The Academy of Natural Sciences, Philadelphia, and The American Ornithologists’ Union, Washington, DC. Palacios, E. and Mellink, E. (1996) Status of the Least Tern in the Gulf of California. Journal of Field Ornithology 67, 48-­‐58. Powell, A.N. (2001) Habitat characteristics and nest success of Snowy Plovers associated with California Least Tern colonies. Condor 103, 785-­‐792. Székely, T., Kosztolanyi, A. and Küpper, C. (2008) Practical guide for investigating breeding ecology of Kentish plover Charadrius alexandrinus, University of Bath. Thomas, S.M., Lyons, J.E., Andres, B.A., ElliotT-­‐Smith, E., Palacios, E., Cavitt, J.F., Royle, J.A., Fellows, S.D., Maty, K., Howe, W.H., Mellink, E., Melvin, S. and Zimmerman, T. (2012) Population Size of Snowy Plovers Breeding in North America. Waterbirds 35, 1-­‐14. US Fish and Wildlife Service (1993) Determination of threatened status for the Pacific Coast population of the western snowy plover, pp. 12864–12874, Federal Register. Verhoeven, J.T.A. and Setter, T.L. (2010) Agricultural use of wetlands: opportunities and limitations. Annals of Botany 105, 155-­‐163. 13