Coastal Management

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The Demise of a Tropical Coastal Lagoon as Breeding Habitat for Ground-Nesting Waterbirds: Unintended, but Anticipated Consequences of Development

Eric Mellink & Mónica E. Riojas-López

To cite this article: Eric Mellink & Mónica E. Riojas-López (2017) The Demise of a Tropical Coastal Lagoon as Breeding Habitat for Ground-Nesting Waterbirds: Unintended, but Anticipated Consequences of Development, Coastal Management, 45:3, 253-269, DOI: 10.1080/08920753.2017.1303766 To link to this article: https://doi.org/10.1080/08920753.2017.1303766

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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=ucmg20 COASTAL MANAGEMENT 2017, VOL. 45, NO. 3, 253–269 http://dx.doi.org/10.1080/08920753.2017.1303766

The Demise of a Tropical Coastal Lagoon as Breeding Habitat for Ground-Nesting Waterbirds: Unintended, but Anticipated Consequences of Development

Eric Mellinka and Monica E. Riojas-Lopez b aDepartamento de Biologıa de la Conservacion, Centro de Investigacion Cientıfica y de Educacion Superior de Ensenada, Ensenada, Baja California, ; bDepartamento de Ecologıa, CUCBA, Universidad de Guadalajara, Zapopan, Jalisco, Mexico

ABSTRACT KEYWORDS Laguna Cuyutlan (, Mexico), an Important Bird Area, used to conservation; Laguna provide breeding habitat for ground-nesting waterbirds. During 2014 Cuyutlan; Laridae; Mexico and 2015, nesting efforts of laughing gull, black skimmer, and royal, gull-billed and Forster’s terns failed almost completely due to inundation, while least terns and snowy plovers fared the same during 2014. No anomalies in rainfall, tidal level, or coseismic subsidence explained such failure. Rather, the inundations were due to the enlarging of Canal Tepalcates that connects the lagoon with the sea, which was widened from 100 to 300 m and dredged to 17-m deep. Before this, the hydrodynamics were regulated by evaporation and runoff. Now, increased seawater volumes dominate the basin’s hydrodynamics. The failure of Laguna Cuyutlan as a breeding habitat for these birds is an important threat for these species, as this lagoon held one of the < 20 colonies known for several of these species along the western coast of North and Central America. Documenting this demise of Laguna Cuyutlan for ground-nesting waterbirds transcends the regional scale as it emphasizes the little consideration still given to biodiversity vs. economic development, and is a warning for coastal projects in other developing areas of the world.

Introduction Coastal lagoons are one of the most productive ecosystems on earth, providing a wide range of ecosystem services and resources. However, many of them rank among the most threatened aquatic ecosystems, mostly due to human-caused habitat loss and modification (Millennium Ecosystem Assessment (MEA) 2005; Kennish and Paerl 2010). Aquatic birds are specially impacted by this, and 21% of all wetland-dependent bird species are globally threatened, especially those in coastal areas (MEA 2005). The 7828 km of the west coast of Mexico include 88 of the country’s 164 coastal lagoons (Ortiz and De la Lanza 2006. As elsewhere in the world (Day et al. 1989;Alongi 1998; Kennish and Pearl 2010), these coastal lagoons provide critical ecosystem services,

CONTACT Eric Mellink [email protected]; [email protected] P.O. Box 430222, San Diego, CA 92143-0222, USA. Supplemental data for this article can be accessed on the publisher’s website. © 2017 Taylor & Francis 254 E. MELLINK AND M. E. RIOJAS-LOPEZ including the regulation of biochemical processes, sediment stabilization, coast protec- tion, protein resources for the local population, and nursery habitat for marine fish and invertebrates of commercial importance. These lagoons provide habitat for numerous resident and migratory wildlife species, including at least 40 species of coastal birds, some with conservation problems, which nest in them (Howell and Webb 1995). Despite the overall biological importance of coastal systems, in Mexico they have received little protection beyond being listed as Ramsar sites and the legal protection of mangroves (http://www.ramsar.org/es/humedal/mexico, accessed 13 Jan 2017; SEMARNAT 2003), and many have been deprived of fresh water, suffered hydrological alterations, and received increased sediment volumes, agrochemicals or urban pollutants, and alien species (v.gr. Mellink and Riojas-Lopez 2009). As a result of reduced freshwater flows, pollution, and transformation to shrimp aquaculture, urbanization and tourist development along the coasts, >62% of Mexican wetlands have been lost (Lara-Lara et al. 2008; Landgraveand and Moreno-Casasola 2012). Some anthropogenic impacts on coastal wetlands in Mexico are irreversible, and the remediation of significant area of wetlands would incur large economic, political, and/ or social costs, and is therefore unlikely. Hence, reversal, or even reduction of impacts upon coastal systems is not foreseen in the near future; rather, it seems that human- induced deterioration is accelerating. Even further, in addition to local anthropogenic stressors upon these systems, they will be impacted strongly by the global climate change currently developing, largely through rising sea levels (Galbraith et al. 2002; Poff,Brinson,andDay2002;Erwin2009). The study of the ecological processes in coastal wetlands, and the documentation of human impacts upon them should be a pri- ority as such knowledge should be the base for designing management actions that help them continue to provide environmental services. This is imperative in view of the large-scale environmental changes anticipated due to aggressive development pressures. The impact of these large-scale changes can often be counteracted by local solutions, which reinforces the importance of generating information at the local scale. Laguna Cuyutlan (Figure 1), on Mexico’ssouthernPacificcoast,isan80£ 14-km long coastal lagoon in the middle of a long stretch of coast lacking other major coastal lagoons. It is highly relevant for waterbird conservation (Mellink and Riojas-Lopez 2009), and has been recognized as an “Area de Importancia para la Conservacion de las Aves” (Important Bird Area) (AICA Technical Committee in. lit. 2014). Culturally, it has been important since pre-Hispanic times for the production of salt, which is still done today (Ewald 1985). The eastern section of this lagoon (Basins III and IV; Figure 1) has been designated as a Ramsar site, but its western part (Basins I and II) has not, coinciding with strong governmental interests in developing a large, industrial port in them. Indeed, the Land Management Plan for the area (2003) that did not allow for such development was modified in 2007 to do so. The new development focused on the expansion of the port of Manzanillo into Basin II of the lagoon. The first step of this port expansion was the construction of a liquefied natural gas facility. It would have a storage capacity of 559,325.89 barrels/ month, and a distribution capacity of 10,000 barrels/day; the gas would be provided from tanker ships anchored offshore through marine tubes, and distributed by tanker trucks (Environmental Impact Statement, January 2004). A subsequent liquefied gas terminal was proposed in 2005–2006 (Environmental Impact Statement, undated). It COASTAL MANAGEMENT 255

Figure 1. Laguna Cuyutlan, Colima, and its environs (Image source: Google Earth, © 2014 DigitalGlobe. Reproduced by permission of DigitalGlobe. Permission to reuse must be obtained from the rightsholder.). included the dredging and widening of Canal Tepalcates, an artificial, clogged connec- tion between the lagoon and the sea, to allow entrance of gas-carrying tankers. One of the three options for this project, option “Omega,” which required the construction of a levee between the enlarged canal and gas terminal and the lagoon, was authorized (Letter S.G.P.A./DGIRA.DG.0465.08, signed by the director of the Direccion General de Impacto y Riesgo Ambiental, SEMARNAT, 11 February 2008). Canal Tepalcates was widened and deepened in 2011–2012, but the levee was not built.

Hydrology of Laguna Cuyutlan Laguna Cuyutlan has suffered many anthropogenic modifications since the late 19th century (Mellink and Riojas-Lopez 2007), but their effect on the hydrological attributes of the lagoon have not been studied. Even the environmental impact assessment required for the approval of the opening of Canal Tepalcates is quite poor on this subject. From maps drawn in the 19th century and early 20th century (Haroort 1834;Banda 1848;Garcıa y Cubas 1858;MatuteandOrozco1865; Matute 1862;Harivel1900;Santa- Cruz 1900) it is clear that at that time the lagoon functioned like a typical, pristine, trop- ical coastal lagoon in which the main hydrological driver was the summer rains, which 256 E. MELLINK AND M. E. RIOJAS-LOPEZ

Figure 2. Climograph of the Colima coast (Manzanillo airport weather station). account for >90% of the annual rainfall of 800–864 mm (Figure 2). During the dry sea- son a wave-induced sand bar would close the mouth of the lagoon, preventing water interchange with the sea. During the rainy season, floodwater would pile up inside the lagoon until finally breaking through the mouth, lowering water levels and salinity, and scouring sediments accumulated inside the lagoon (Yanez-Arancibia~ 1978). Since 1922, and especially since 1950, Rıo Armerıa, the main river that discharged fresh water in Cuyutlan, was diverted to create the Tecoman agricultural district (Serrano Alvarez 1999; Mellink and Riojas-Lopez 2007). This altered the cycle of flooding and draining and the fluctuations in salinity of the system. Flow through the natural connection with the sea, the mouth of the Estero Palo Verde (Figure 1), was probably very restricted as a conse- quence. Currently the flow is negligible as the mouth is permanently closed due to the devel- opment of a small community of beach-side eateries. Later, two artificial connections with the ocean were constructed, one to provide cooling water for the thermoelectric facility, and the other, Canal de Tepalcates, to provide a connec- tion that allowed water interchange with the sea to enhance the production of shrimp and fish in the lagoon (Mellink and Riojas-Lopez 2007). The latter soon clogged with wave-car- ried sediments. Artificial dredging of Canal de Tepalcates followed by natural clogging occurred at least thrice in the ensuing decades. By the early 21st century, the lagoons hydrological dynamics was driven by local phenom- ena. During the fall and winter water levels rose due to local rainwater runoff, and during the late winter and spring the lagoon slowly desiccated by evaporation, leaving very low water levels and a number of exposed, muddy islets and shores (Figure 3). During the remainder of the year some fresh water reaches the lagoon from underground seeps, but its effects appear to be local, although they remain unstudied. As part of the environmental impact statement (EIS) documents for the gas facilities, in the early 21th century the hydrology of Laguna Cuyutlan was defined by the presence of nat- ural and artificial barriers and a bathymetry modified by seaway openings and silting, among others. In these documents it was argued that the lagoon lacked ecological integrity and was COASTAL MANAGEMENT 257

Figure 3. Muddy islets and shore mudflats used for nesting by waterbirds in Laguna Cuyutlan, Colima, (indicated by white arrows) before and after the onset of summer rains (10/06/2009 left, and 13/07/2009 right). Between both dates, the area received rain from Tropical Depression E1, Hurricane Andres, and Tropical Storms Blanca and Dolores (Image source: Google Earth, © 2016 DigitalGlobe. Reproduced by per- mission of DigitalGlobe. Permission to reuse must be obtained from the rightsholder.). doomed by silting, as a result of re-direction of Rıo Armerıa, and that the construction of a connection with the sea was critical to revitalize the system; otherwise, the system would dis- appear. This same view has been held by government fishery scientists (e.g., Ascencio- Borondon, Solis-Gil, and Coba-Cetina 1987; Mena-Herrera 1979). The only known hydrological study of the lagoon was performed in 2004–2008 for the EIS, and was based on a bathymetric survey and mathematical modeling. The model showed that enlarging and dredging Canal Tepalcates would cause the mean water level in Basin III to rise 32–39 cm, but during high spring episodes the water level would be much higher, while the variation range would increase in 370% (Avila Escobedo and Lara Hernandez 2010). Both, in this study and in the EIS, the restoration of fresh water flows into the lagoon was not considered, and the several publications on waterbirds available were neglected.

Ground-nesting birds of Cuyutlan Little information on Cuyutlan’s waterbirds or on any other wildlife exists from the time when it was subject to pristine dynamics, except for information on crocodiles which were abundant in the mid and late 20th century (Anonymous 1850; Rodriguez 1896). In the early 20th century, within the context of southern Mexico, Laguna Cuyutlan was an important site for wintering waterfowl (Leopold 1977; Saunders and Saunders 1981), but in the 1950s the large waterfowl numbers in the lagoon plummeted, arguably due to the loss of fresh water input after Rıo Armerıa was intervened (Mellink et al. 2009). The mangrove communities of southwestern Mexico provide habitat for the nesting of several species of wading birds. Laguna Cuyutlan was considered one of the 19 most valuable waterbird nesting sites in western Mexico (Knoder, Plaza, and Sprunt 1980). Currently, eleven of such species nest in Basin III of this lagoon: great egret (Ardea alba), little blue egret (Egretta caerulea), snowy egret (E. thula), tricolored heron (E. tricolor), blackcrowned night-heron (Nycticorax nycticorax), yellow-crowned night-heron (Nyctanassa violacea), green heron (Butorides virescens), cattle egret (Bubulcus ibis), roseate spoonbill (Platalea ajaja), white ibis (Eudocimus albus) and wood stork (Mycteria americana), in addition to neotropic cormorant (Phalacrocorax brasilianus) (Mellink and Riojas-Lopez 2008; 2009; 258 E. MELLINK AND M. E. RIOJAS-LOPEZ

Riojas-Lopez and Mellink 2016) and black-bellied whistling duck (Dendrocygna autumnalis) (Unpubl. data). Magnificent frigatebird (Fregata magnificens) was recorded nesting in the late 1970s (Knoder, Plaza, and Sprunt 1980; possibly in basin II, where they may still nest). The wood stork colony in the lagoon was established in 2014 and it is the only colony of this species formally reported from western Mexico in the last 35 years (Riojas-Lopez and Mellink 2016). The list of canopy-nesting species is increased by species nesting elsewhere in the lagoon, but for which no data have been published. Ground-nesting waterbirds were an important class of Laguna Cuyutlans nesting bird assemblage. Snowy plovers (Charadrius nivosus), Wilson’s plovers (C. wilsonia), black- necked stilt (Himantopus mexicanus), laughing gulls (Leucophaeus atricilla), royal (Thalas- seus maximus), least (Sternula antillarum), gull-billed (Gelochelidon nilotica) and Forster’s terns (Sterna forsteri), and black skimmer (Rynchops niger) nested on muddy islets and shores (Mellink and Riojas-Lopez 2005; 2006; Mellink, Palacios, and Amador 2007; Mellink, Riojas-Lopez, and Luevano 2009; Palacios and Mellink 2007), while the clapper / king rail (Rallus longirostris / elegans; Howell 1994; Howell and Webb 1995) nested in marsh vegeta- tion (Batis maritima). For five of these ground-nesting species, Cuyutlan was particularly relevant. In 2005 the breeding population of the vanRossem’s gull-billed tern (G. n. vanrossemi) was estimated at 526 breeding pairs at only 13 sites in western Mexico and southwestern United States (Palacios and Mellink 2007; three colonies were added later; Mellink, Riojas-Lopez, and Luevano 2009; Hernandez-Vasquez et al. 2015). The Forster’s tern colony represented a leap of >1,700 km from the nearest Pacific Coast colony (Mellink and Riojas-Lopez 2006) and is currently one of only three confirmed colonies in Mexico (Gomez del Angel, Palacios, and de Sucre-Medrano 2015). Royal terns and black skimmers were known to nest at only a few locations along west- ern Mexico (Mellink, Palacios, and Amador 2007; Mellink and Palacios unpublished data). Laughing gulls, although summing up to thousands of pairs in western North America, are known to nest at only a few locations, one of which is Laguna Cuyutlan (Howell and Webb 1995), where 10,000 were nesting in the late 1970s (Knoder, Plaza, and Sprunt 1980). Of all the waterbird species breeding in Laguna Cuyutlan, the woodstork (special protec- tion), pelican (threatened subspecies), snowy plover (threatened), least tern (special protec- tion), and rail (threatened, whichever the local subspecies is) are officially considered at risk (SEMARNAT 2010). However, no actual population estimates for these species exist for southern Mexico to assess the relative importance to them of Laguna Cuyutlan. To date, no other wetland in southern Mexico supports such a rich array of breeding waterbird species. The largest wetland systems in southwestern Mexico are Marismas Nacio- nales, in Nayarit and Sinaloa, the Laguna Potosı complex, in , and the Itsmo de Tehuantepec wetlands, in and Chiapas. Marismas Nacionales has been touted for its bird diversity, but is most important due to its winter use by migratory shorebirds. Informa- tion on breeding waterbirds is limited, although snowy plover, royal tern, gull-billed tern, and black skimmer, in addition to some waders (data not published) nest there; El Potosı supports nesting of snowy plover, collared plover, Wilsons plover, killdeer, gull-billed tern, least tern and, apparently, black skimmer, but the latter has not been confirmed; while the Istmo de Tehuantepec wetlands support the nesting of black skimmer (Mellink and Riojas- Lopez 2005; Mellink, Palacios, and Amador 2007; Mellink, Riojas-Lopez, and Luevano 2009; Palacios and Mellink 2007). Other wetlands have 4 or less ground-nesting species (Mellink, Riojas-Lopez, and Luevano 2009). Oaxacan coastal wetlands, although insufficiently COASTAL MANAGEMENT 259

Figure 4. Canal Tepalcates before (22/04/2011) and after (26/03/2013) it was enlarged (Image source: Google Earth, © 2016 DigtalGlobe. Reproduced by permission of DigitalGlobe. Permission to reuse must be obtained from the rightsholder.). surveyed, support breeding canopy-nesting waders, but few ground-nesting waterbirds (Mellink, Luevano, and Zuria 1998). In March 2012, Canal Tepalcates was dredged again, but this time to a depth of 17m, and was widened from 100 to 300 m (Figure 4). In 2014 and 2015, we carried out field work to monitor the ground-nesting waterbirds breeding in Basin III. In this contribution, we com- pare field data we obtained in 2014 and 2015 on ground-nesting waterbirds in Laguna Cuyutlan, with data we obtained in 2003, 2004, 2005, and 2010.

Methods We had surveyed Laguna Cuyutlan’s Basin III to the extent that could be accessed with a skiff (minimum water depth »25 cm), as well as some of the adjacent mudflats, on 20/05/2003, 12/05/2004, 23/04/2005, 14/05/2005, 23/05/2005, 3-4/06/2005, 2/07/2005, 12/06/2010, and 27/06/2010. We used the skiff to get close to the islets, and then inspected these with binocu- lars and if colonies were present, we tried to reach them on foot. When soft mud prevented reaching the colonies on foot, the birds in them were identified and counted from the skiff. Shore sites were visited by car and on foot. Most of our relevant data from these surveys has been published (Mellink and Riojas-Lopez 2005; 2006; 2008; Mellink, Palacios, and Amador 2007; Mellink et al. 2009; Palacios and Mellink 2007). During the breeding season of 2014 we surveyed the area on 14–15/04, 12/06, and 12/07, and during 2015 on 15/04, 13/05, 22/06, and 22/07 (hereafter, for reading convenience, dates will be referred to as month/year). On the April 2014 visit, we searched all traditional nesting areas that could be reached by skiff, and inspected the area with binoculars and spotting scope from the top of Mogote Prieto, a rocky island in Basin III. We also examined the far end of Basin III along a ditch that protects salt pans. On the two later 2014 trips, after first scrutinizing the islets from the top of Mogote Prieto we visited those that had birds on them. In April 2015 we searched all potential islets in the center of Basin III, and in May we explored this area and, allowed by the high water level, we also explored much deeper into Basin III than ever previously. In June and July we examined the potential nesting islets from the tip of Mogote Prieto, and surveyed the only colony detected. This year, a 360-m^2 area of the San Buenaventura salt pans that was left idle and was protected from inundation by active salt pans with raised levees, provided nesting habi- tat for least terns and snowy plovers. We surveyed this site from May to July. 260 .MLIKADM .RIOJAS-L E. M. AND MELLINK E.

Table 1. Ground-nesting waterbirds in the western section of Laguna Cuyutlan’s Basin III, Colima, Mexico.

Species High count Usual 2014 2015

Mud islets Laughing Gull 10,000 indiv. (1970s; Knoder, Several hundred to low thousand <250, most failed, but some re-nesting <200, most failed, but some re-

Plaza, and Sprunt 1980) nesting OPEZ Royal Tern »1100 (2004) Several hundred Several nesting attempts, failed due to Several nesting attempts, failed due inundation to inundation Black Skimmers 196 (2005) Several tens to low hundreds Apparent nesting attempts, failed due to Apparent nesting attempts, failed inundation due to inundation Gull-billed Tern 55 (2005) Low tens April nesting attempt, inundated, April nesting attempt, inundated, abandoned afterwards abandoned afterwards Forster’s Tern 8 (2005) <10 None detected One nest with 4 eggs in April. One adult with 2 fledglings in June. Black-necked Stilt — 10–20 pairs Several, not counted Several pairs with young / juveniles Clapper Rail Usually nesting at the fringe One nest w/8 eggs, possibly successful Two pairs with foraging chicks of the lagoon San Buenaventura Salt pans Least Tern 21 (2005) 10–20 pairs Habitat inundated 15 pairs; several young. Snowy Plover <10 pairs <10 pairs Habitat inundated »5–6 pairs. Several young Wilson’s Plover No recorded before 0 Habitat inundated 2 adults C 1 & 2 chicks

Note. Numbers given are number of pairs, unless otherwise stated. Unless indicated, the data were gathered by us. COASTAL MANAGEMENT 261

On each visit during both years we measured salinity with a hand-held seawater refrac- tometer (RHS-10ATC) and water depth, at 3–4 different places in the northwestern section of Basin III. We examined the passage between Basins II and III on December 1–2, 2014.

Results No water level records or measuring devices exist in the lagoon, but, by reference with the San Buenaventura salt pans, our skiff landing place and the base of Mogote Prieto, it was clear that on all 2014 and 2015 surveys, Basin III had water levels 3–4 decimeters higher than the highest we had ever seen previously. These higher water levels coincided with reproductive failure in laughing gull, black skimmers, and royal and gull-billed terns nesting on mud islets, and in least tern, and snowy and Wilson’s plovers on mudflats at the margins of Basin III, when unprotected from such water levels (Table 1, Supplementary data). For- ster’s tern, black-necked stilt, and clapper rails had some nesting success. Laughing gulls had new eggs on every visit until the end of the breeding season, but almost no chicks, which indicates repeated breeding failures. Royal and gull-billed terns commenced nesting in both years, but their colonies were inundated and the eggs drowned. They abandoned Basin III in April/May each year. Nesting of black skimmers was suggested in 2014 by them standing passively near what would have been suitable nesting substrate, but that substrate was inundated; and in 2015 by colony defense behavior of an inundated mudflat. As black skimmers nest on the lowest part of the mudflat which was below a few decimeters of water, no nesting evidence was found. Forster’s terns nest in very low numbers in Cuyutlan’s Basin III, so the lack of records in 2014, and only one nest and 2 fledglings records in 2015, although despairing, is not conclusive. The black-necked stilt is a common species in the area, nesting at the fringes of islets and mar- gins of Basin III, and has not been a focus of our study. In 2014 and 2015 there were several groups of adults performing distractive behaviors, as well as young and juveniles. To some degree, at least, they seemed to have been able to cope with the current inundation levels. Clapper rails regularly nest among the vegetation at the margins of the lagoon, but under current high-water conditions, that habitat is often covered with >20 cm of water, which might have prompted some of the birds to move to mud islets, where there was no record of them nesting before. In July 2014 a nest we had found on June 2014 had disappeared, but givenanincubationperiodof29 days, the chicks being highly precocial, and the capability ofparentstotakesmallchicksontheirbacksifwaterlevelrises,(Rushetal.2012)itisrea- sonable to assume that their reproduction had been successful. The young of this species that we saw in 05 2015 supports this possibility. Despite these two events, we cannot assert whether the majority of clapper rails were able to cope successfully with the higher water lev- els. Finally, least tern, and snowy and Wilson’s plovers, which nested in idle, but protected salt pans, also point at the negative impact of the higher water levels in 2014 and 2015 than before. It was only when adequate substrate (idle salt pans, protected from inundation, in 2015) was available that they nested successfully.

Discussion Clearly, there were catastrophic failures in the reproduction of ground-nesting waterbirds in 2014 and 2015 in Laguna Cuyutlan’s Basin III. High water levels inundated their colonies, 262 E. MELLINK AND M. E. RIOJAS-LOPEZ causing severe to complete breeding failures of gull-billed terns, royal terns, and black skimmers, while laughing gulls had very low success and Forster’s terns and clapper rails, had some. In the case of laughing gulls, the time elapsed between consecutive visits was greater than the 22–27 days required for incubation. So, the lack of chicks, along with finding most or all nests wet and the eggs drowned on every visit, indicates consecutive re-nesting attempts throughout the breeding season in both years. The failures did not come from physiological problems, as the number of eggs per nest was normal and their weight and color were also normal; rather, the failures were caused by the drowning of eggs. This is sus- tained also by the fact that the few re-nesters built nests on the highest available places on the saltwort, with a lower inundation risk but with a higher predation risk (Gonzalez- Medina, Castillo-Guerrero, and Mellink 2009). Black-necked stilts apparently fared better, although we lack solid data to confirm it. Least terns, and snowy and Wilson’s plover repro- duction failed in 2014, at least at San Buenaventura, which was inundated. In 2015, both spe- cies benefited from the accidental early inundation which rendered some salt pans idle, and which were protected from further inundation by active salt pans with raised levees between them and the lagoon. The loss of Laguna Cuyutlan as breeding habitat for ground-nesting waterbirds has nega- tive consequences for the conservation of Mexico’s biodiversity, as this lagoon held one of the <20 colonies that existed along the entire western coast of North and Central America for gull-billed and royal terns, black skimmers, and laughing gulls. The Forster’s tern colony was one of only three recently confirmed active colonies in Mexico. Clapper rails and snowy plovers are officially considered threatened by the government of Mexico (SEMARNAT 2010), and the Laguna Cuyutlan is the southernmost known nesting locality of Wilson’s plovers on the Pacific coast of Mexico. The April 2014 and 2015 situation contrasted with all our previous visits in April and May (12/05/2004, and 23/04/, 14/05/, and 23/05/2005), none of which exhibited signs of inundation at any of the ground-nesting waterbird colonies (Table 2). The widening and deepening of Canal Tepalcates was our main suspect for the reproductive failure, but we will first examine three alternative possibilities. The first scenario causing high water levels within Cuyutlan’s Basin III has to do with rain. Although the major historical venue of fresh water to the lagoon was severed in the 1950s, some rainwater runoff still reaches Basin III. Salinity values in the lagoon reflect such runoff, as from April to July there was a decrease in water salinity inside Basin III (Figure 5) following the onset of the summer rainy season. Ground-nesting waterbirds in Basin III breed during the dry season, between March and April, and the onset of rainy season. Once the rainy season starts, direct rainfall as well as runoff into the lagoon causes the end of the breeding season of ground-

Table 2. Development of the breeding of ground-nesting waterbirds in Laguna Cuyutlan’s Basin III, between 2003 and 2014. All visits were at Spring tides or less than 8 days after them.

Preceded by heavy rainfall and storms

No (April and May) Yes (June and July)

2003–2010 Widespread and successful (2003, 2004, and 2005) Partially inundated, but no drowning (2005,and 2010) 2014, and 2015 Small and drowned Mostly failed COASTAL MANAGEMENT 263

Figure 5. Water salinity from mid-April to mid-July 2014 and 2015 in Basin III, Laguna Cuyutlan, Colima. nesting waterbirds (as well as the end of the salt-production season). Within this period, any 5–6-week period of low water level would allow successful breeding by all the waterbird species that nest on the ground in Laguna Cuyutlan (maximum incubat- ing periods are 31 days for the royal tern, and 32 days for the snowy plover). So, an early onset of the rainy season or unusually strong late-winter rains, which sometimes happen into March, might affect the breeding birds. However, summer rainfall could not explain completely the high water levels found in 2014 and 2015, as even on 18/ 07/2003, when 150»200 mm of rain had already fallen, there were no signs of colony inundation comparable to those in 2014 and 2015. Hence, our first adverse scenario would consist of rains in the spring and/or the early onset of the summer rains in such a way that the time lapse between high water levels caused by rain is not large enough for the birds to nest successfully. The nearest meteorological sta- tion is at Venustiano Carranza (192026.600 N, -1046036.200 W), »5 km north of Basin III, but has recorded time series of data from only the following periods: 2008–2011, 2014 and 1/01–17/03/2015). We obtained complementary data from the station at Armerıa (1854052.700 N, -1035809.200 W), »18 km to the SE of Basin III (data for both at http:// clima.inifap.gob.mx/redinifap/). Clearly, rain pattern in 2014 fell within the long term pattern (Figure 6). 2015 was differ- ent, as it had some rain in March, caused by two winter storms (#8 and #9) interacting with a cold front (#41) and Pacific Ocean humidity. Also, hurricanes Blanca (9 June) and Carlos (15 June) crossed the region dropping 154.4 mm of rain in Armerıa. Basin III, however, was spared from this later rain, according to a local informant (J.L. Ramırez pers. com.). In 2015, relatively low salinity in April (39%; Figure 5) probably resulted from the mid-March rains. Afterwards, salinity increased and remained high, reflecting the lack of pluvial runoff. It was not until rain started falling in mid-July that salinity in the lagoon began to decrease. A second scenario for the inundation could occur when tides were higher in the first half of 2014 and 2015 than in previous years, causing higher water levels inside Basin III. 264 E. MELLINK AND M. E. RIOJAS-LOPEZ

Figure 6. Onset of the rainy season, and early rains in 2008–2015 in Laguna de Cuyutlan. Rainfall lasting >1 day was added and is presented as a single bar. (Venustiano Carranza meteorological station, except for 2012–2013 and 18/03–31/07/2015 which were unavailable and are from the Armerıa station). The early–mid June 2015 rain recorded in Armerıa did not reach Basin III (see text) (Source: http://clima.inifap.gob.mx/redinifap/).

Inundation of the islets after May/June is not surprising, as it is the standard of the area, although even after May/June we had always found lower water levels than in 2014 and 2015. Before 2010 the predicted highest tide immediately ahead of our visits was 4.27 § 0.24-m high, and the real (adjusted) tides were 4.26 § 0.24-m high. From 2011 to 2014, predicted and observed values were 4.29 § 0.15 and 4.37 § 0.21m, respectively. In neither case were the observed tidal heights different from the pre- dicted ones. The 6-cm higher average of the post-2011 tides is largely due to the 12/ June/2014 tide which was 32 cm higher than predicted, as a result of Hurricane Cris- tina which pushed water against the edge of the continent. Although this larger mid- June tide could have influenced water levels inside Basin III, inundation of colonies COASTAL MANAGEMENT 265 had already happened. Clearly, differences in tide level, as compared to previous years, can also be discarded as a cause of the 2014 and 2015 inundation of the islets on which ground-nesting waterbirds in Laguna Cuyutlan’sBasinIIInest. A third scenario is as follows. The Colima plain, on which Cuyutlan lays, is subject to coseismic deformation (ground deformation caused by an earthquake), and during the October 9, 1995 earthquake, the entire plain dropped 11.8 cm (Ortiz-Figueroa et al. 2000). Increased relative tidal levels due to coseismic subsidence would be a pos- sible cause for higher than previous inundation levels in Laguna Cuyutlan. However, the Cuyutlan plain has currently been pushed up to its former level (Modesto Ortiz- Figueroa pers. comm.), and although a very large earthquake centered at nearby Tecoman shook the region on January 21, 2003, no subsidence happened. Thus, an increase in relative water level inside the lagoon in 2014 due to coseismic subsidence did not occur. Anomalies in rainfall, tide height, and coseismic subsidence having been discarded, the enlarging of Canal Tepalcates is the most logical explanation for the early and high levels of inundation of nesting islets in Cuyutlan’s Basin III and the consequent breeding failure by ground-nesting waterbirds. No hydrodynamic data are available, but prior to its enlarging, the clogged and narrower Canal Tepalcates presumably restricted the amount of water that entered the lagoon during high spring tides, hav- ing minimal effect on Basin’sIIIwaterlevelwhichwasregulatedmostlybyevapora- tion and pluvial runoff. With the enlarging of Canal Tepalcates, much more water would enter during spring tides. Although this effect is by itself enough to explain the 2014 and 2015 breeding failures in Basin III, this effect could be enhanced when storms cause seawater to pile up against the coast. This happened during the mid- June/2014 spring tides, when Hurricane Cristina caused a tide 32 cm above the pre- dicted value at the Manzanillo Pier, and the 15/06/2015 spring tides, when waves were predicted to be 2–3 m higher than normal due to Hurricane Carlos. After the now augmented water volume flows into Basin III due to the enlarged Canal de Tepalcates, water level remains high inside Basin III due to the damming effect of the debris of the 2003 collapse of the highway bridge that spanned the water passage between Basins II and III, resulting in shallow, sediment-filled area at the mouth of the latter (no bathymetric work on this section of the lagoon is available but it is visible clearly in Google Earth images). This “levee” prevents complete drawdawns during low tides, as reflected by the water level inside Basin III on June 11–12, 2014 being close to maximum spring tide of the tidal cycle (slightly higher tides were predicted for the two next days). The highest predicted tide at the Manzanillo pier that day was 83 cm above mean low water level (mlwl), while the lowest pre- dicted tide was 22 cm below mlwn, thus there was >1 m of vertical variation in tide level at sea. However, the water level recorded by an automatic camera deployed at the shore of Basin III exhibited a vertical variation of only a few centimeters between these two events (Figure 7). We have no data on how current conditions will affect other waterbirds, like shorebirds, waders and waterfowl, that use or used Laguna Cuyutlan’s Basin III. It seems likely that shorebirds might have much less foraging habitat and might be, accordingly, found at lower numbers now than before. As for waterfowl, fresh water in the lagoon was, reportedly, a crit- ical factor in providing good habitat for them, and its drastic reduction led to the collapse of waterfowl winter populations (Mellink et al. 2009). This appears to be associated with 266 E. MELLINK AND M. E. RIOJAS-LOPEZ

Figure 7. Inundation level at 19.01N, 114.19 W, near highest (11/06/2014, 16:00 hr, upper) and lowest (12/06/2104, 9:00 hr, lower) spring tides, as recorded by an automatic camera. increased seawater volumes, as salinity in Basin III is much higher than when it was an important waterfowl site, making the basin even less favorable for them. The current condition in Laguna Cuyutlan was not unexpected, as the effects of the open- ing of large waterway connecting Laguna Cuyutlan had been anticipated (Mellink and Rio- jas-Lopez 2009): “Probably the most serious threat… is a long term modification of the water levels, especially increases… [t]he islets and salt flats on which Charadriiformes nest could disappear… [t]he permanent opening of an artificial channel might cause such condi- tions…” and “The re-gasification plant and the future port development [should] at least include a levee to prevent alterations in water level in as large a section of the lagoon as pos- sible, including the totality of Basins III and IV.” A levee was indeed planned. The named “Plan Omega” included a large levee surround- ing the enlarged canal and the gas terminal, apparently to prevent accidental spillage of pol- lutants from ships into the surrounding wetland. However, the levee was not built. Administrative records are not publicly available, so that is it not clear whether this resulted from the argument that spillage risks and consequences were minimal, or followed the long- held argument by fishery scientists that a connection between sea and lagoon would be bene- ficial for the latter, or was due to potential interference with plans for a large port develop- ment. Notwithstanding these reasons, it is now highly unlikely that a levee around the enlarged Canal Tepalcates and gas plant be built to keep the value of Basin III for ground- nesting waterbirds and for salt producers. Alternative actions must, thus, be implemented. Possibilities are: (1) restrict water entrance to Basin III, though levees and lock gates at its mouth, (2) elevate nesting islets arti- ficially, maybe by piling mud on them, (3) construct artificial floating islets and (4) for least terns and snowy plovers, pay for some of the salt pans adjacent to the water not to be used and raise their edges to prevent inundation. While no specific management actions are taken, Laguna Cuyutlan’s Basin III has ceased to be valuable for ground-nesting waterbirds as a result of increased water levels caused by enlarging the major connection with the sea. The formally published inventory of nesting birds of Laguna Cuyutlan is much larger and richer than that of other coastal wetlands of tropical Mexico, which reaffirms the relevance of this lagoon for waterbird conservation and the urgency to implement a management strat- egy to reverse the negative impacts to its nesting waterbirds. Other coastal systems may be as COASTAL MANAGEMENT 267 rich as Cuyutlan, but they have not been surveyed or relevant information has not been pub- lished. Raising the issue of the impacts by increasing seawater flow on Cuyutlan’s waterbirds provides lessons to prevent the loss of habitat for nesting waterbirds in other coastal lagoons, in the face of future development projects. Documenting this demise of Laguna Cuyutlan for ground-nesting waterbirds emphasizes at least two greater-scale issues applicable to developing countries throughout the world. First is the little consideration given to biodiversity (and, in this case, rural welfare and eco- nomic development as well) when it comes to “national” development interests, especially for high-priority sectors, such as energy. In the case of Cuyutlan, protection of birds and salt pans would have required a minor budget increase within the overall costs of enlarging Canal de Tepalcates and re-locating the entire railroad track in Basin II, but the issue was completely neglected. Second, large-scale development in coastal wetlands can impact nearby systems which, because they are not the project’s target area, are not covered in any EIS or other similar legal instruments. Special attention should be paid to prevent such unin- tended, off-site impacts.

Acknowledgments

We thank two anonymous reviewers for comments that helped to improve this article and Paolo Solano for providing important reports.

Funding Field work was made possible by internal funds from the Centro de Investigacion Cientıfica y de Edu- cacion Superior de Ensenada and by personal resources of the authors.

References

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