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Ocean & Coastal Management 96 (2014) 12e19

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Ocean & Coastal Management

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Restoration of a degraded coral reef using a natural remediationprocess: A case study from a Central Mexican Pacific National Park

J.J.A. Tortolero-Langarica, A.L. Cupul-Magaña, A.P. Rodríguez-Troncoso*

Laboratorio de Ecología Marina, Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad de Guadalajara,Avenida Universidad No. 203, Puerto Vallarta, CP 48280 Jalisco, Mexico

a r t i c l e i n f o

Article history:Available online

* Corresponding author. Tel.: þ52 3222262319.E-mail address: pao.rodriguezt@gmail.com (A.P. R

http://dx.doi.org/10.1016/j.ocecoaman.2014.04.0200964-5691/� 2014 Elsevier Ltd. All rights reserved.

a b s t r a c t

Facing the worldwide coral degradation, active restorations are moving toward improving techniques tomaintain coral coverage. Transplant methods have been used to restore coral reef areas that werecompletely degraded; however restoration is not commonly employed at coral reefs with evident lossthat may jeopardize the maintenance of the community. In this study the re-attachment concept usingthe natural fragmentation of branched-corals was tested as an accelerator process to natural recoverybased on asexual reproduction. Survivorship, growth and attachment rates of three Pocillopora species onboth natural and artificial substrates were evaluated at four sites of Islas Marietas. Over one year ofmonitoring during 2012e2013, resulted in a high survivorship of 87% on artificial underwater structuresand 67% on natural substrate, the height and radial growth, on both substrata increase 2-fold from theinitial size; although both substrata were viable, coral fragments attach faster on natural (4 months) thanartificial structures (6 months). The results demonstrate that re-attachment using natural substrata is apotential and no invasive instrument for treating coral reefs not completely degraded in restorationprograms.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Coral communities are one of the more complex and importantcoastal environments as numerous marine taxa and economic re-sources depend directly or indirectly on them. Despite theirimportance, corals communities are also one of the most degradedecosystems in recent years caused by natural and anthropogenicthreats (Dight and Scherl, 1997; Glynn, 2000; Hoegh-Guldberget al., 2007; Hoegh-Guldberg, 2011; Pandolfi et al., 2011). Inresponse to the continuous and abrupt decline in coral coverage,there is an urgent need to improve coral reef conservation andmanagement strategies by attempting to mitigate negative impacteffects over coral communities and promoting species recovery(Jordan et al., 1987; Edwards, 1998, 2010; Treweek, 1999). Impor-tant studies have been initiated to maintain and enhance the coralcoverage and reef-associated biodiversity with active restorationand rehabilitation studies, improving different approaches witheffective results such as: 1) coral transplantation (Harriott and Fisk,1988; Yap et al., 1992, 1998; Clark and Edwards, 1995; Omori and

odríguez-Troncoso).

Fujiwara, 2004; Edwards and Gomez, 2007; Gomez et al., 2011);2) coral gardening (Rinkevich, 2000, 2005, 2008, 2014; Shaish et al.,2010; Levy et al., 2010; Lirman et al., 2010; Mbije et al., 2010), 3)artificial underwater structures (Pickering et al., 1998; Precht et al.,2002; Edwards, 2010); 5) electrochemical reef structures (VanTreeck and Schuhmacher, 1997; Schuchmacher et al., 2000, 2002;Sabater and Yap, 2002); 5) coral aquaculture (Petersen and Tollrian,2001; Heyward et al., 2002; Omori et al., 2003) and various othertechniques (Ammar et al., 2000; Baums, 2008) to encourage Gov-ernment agencies, managers, NGO’s and stakeholders to invest andapply active management tools, as local or international legislationand education has not been enough to prevent coral reef deterio-ration with no positive results in conservation and management(Sale, 2008; Rinkevich, 2008).

At Mexican Pacific (MP), the coral communities are character-ized as fringing reef patches of scleractinian corals dominated bythe genera Pocillopora in shallowerwaters and Porites and Pavona indeeper zones (Carriquiry and Reyes-Bonilla, 1997; Reyes-Bonillaet al., 2005). Along the MP, one of the most important coral reefsystems in the Central MP is located at Islas Marietas National Park(IMNP); this region has been affected by several coral bleachingevents with high mortality rates (>90%) (Glynn, 2000, 2001;Carriquiry et al., 2001; Reyes-Bonilla et al., 2002; Cupul-Magaña

J.J.A. Tortolero-Langarica et al. / Ocean & Coastal Management 96 (2014) 12e19 13

and Calderón-Aguilera, 2008) and consequently a considerable lossof coral coverage has been observed, where Pocillopora has beendocumented as the most sensitive to bleaching (Calderón-Aguileraand Reyes-Bonilla, 2006; Carriquiry et al., 2001; Reyes-Bonilla et al.,2002). Recently, as the stress events had becomemore frequent andintense coupled with the anthropogenic pressure, as a result of thissynergic effect, the community has become unable to recover andmaintain the organisms which depend on them; therefore positiveand active human intervention is needed to recovery and guaranteecoral species persistence thought long-term restoration programs(Rinkevich, 2005; Sale, 2008).

So far, in situ long-term restorations have been applied at theEastern Tropical Pacific (ETP) in order to validate restoration stra-tegies that improve management programs (Guzmán, 1991; Liñán-Cabello et al., 2010). However, herein is the first study in the ETPregion that search for non-destructive techniques that wouldimprove coral restoration, and analyze the potential use of Pocil-lopora species using organisms obtained by natural fragmentation(asexual recruits) caused by bioerosion, physical conditions such aswaves, tides and currents. As these factors are natural, the piecesare healthy fragments founded in the same area suitable to be re-attached for restoration without affecting any healthy colonies. Inorder to broaden the conservation and management knowledge ofcoral reefs through restoration experiences that may in turn applyto different locations and regions with similar ecologicalconditions.

In the present study three branched Pocillopora species wereused: Pocillopora damicornis (Linneaus, 1758), P. verrucosa (Ellis andSolander, 1786) and P. capitata (Verrill, 1864), based on theirabundance, dominance and high natural fragmentation in theCentral MP (Carriquiry and Reyes-Bonilla, 1997; Reyes-Bonilla et al.,2005; López-Pérez et al., 2007). This restoration technique wastested using comparisons assessing the effectiveness of using nat-ural versus artificial substrata and the potential of the most abun-dant branching coral species in different locations along IslasMarietas area, using as variables survival, growth and attachmentrates, in order to set up the restoration program in the area and to

Fig. 1. Islas Marietas National Park (IMNP) study site. Isla Larga: Zona de Restauración (ZR)(AM).

promote active conservation and management techniques to pre-serve Eastern North Pacific coral communities.

2. Materials and methods

2.1. Study area

Islas Marietas National Park (20�4003500 e 20�4104500 N,105�3303000 e 105�3801000 W) is located at 7.9 km off the northerncoast of Bahía de Banderas, Nayarit, México (Fig. 1). This NationalPark consists of two islands and several islets volcanic in origin: IslaLarga (48 ha) and Isla Redonda (28 ha), separated by a one kilo-meter water channel (Gaviño and Uribe, 1981). Rock, sand andsmall reef patches predominate at 3e18 m around both Islands(CONANP, 2007). The area is considered as an important coraldispersal connectivity zone over the ETP (Glynn and Ault, 2000), asis influenced by three transitional ocean currents: California Cur-rent (CC) providing cold (w18e21 �C) and rich-nutrients waters,present from January to March (Shea et al., 1992; Kessler, 2006;Pennington et al., 2006; Pantoja et al., 2012); Mexican Costal Cur-rent (MCC) carrying warm (w27e30 �C) and low-nutrients waters,present between July to November; and Gulf of California Current(GCC) adding warm waters with high salinity during mid-summer(da Silva et al., 1994; Kessler, 2006; Pennington et al., 2006;Palacios-Hernández et al., 2010; Pantoja et al., 2012).

The mean annual Sea Surface Temperature (SST) in the area isw27 �C (Shea et al., 1992; Palacios-Hernández et al., 2010), and isinfluenced periodically by water temperature anomalies such asENSO (El Niño-Southern Oscillation) events with both El Niño(þ3 �C SST anomalies) and La Niña (�4 �C SST anomalies) whichcaused major bleaching and mortalities (Fiedler and Talley, 2006;Kessler, 2006; Wang and Fiedler, 2006; Glynn, 2000, 2001;Carriquiry et al., 2001; Reyes-Bonilla et al., 2002; Cupul-Magañaand Calderón-Aguilera, 2008). Besides weather events, Islas Mar-ietas is a popular tourist area declared by the Mexican governmentas a National Park in 2005 (CONANP, 2007), this recognition hasproduced other anthropogenic stresses such as: intensive tourism

and Cueva del Muerto (CM); Isla Redonda: Plataforma Pavonas (PP) and Amarradero

J.J.A. Tortolero-Langarica et al. / Ocean & Coastal Management 96 (2014) 12e1914

activities (tour boats, snorkeling and diving); overfishing and therapid coastal human development that permanently influence thearea. However, active and passive management strategies are stillinactive or limited, compromising the conservation of coral com-munities in IMNP.

2.2. Growth and attachment rates

Based on the higher coral coverage of Pocillopora colonies andthe availability of natural fragmented corals, four sites wereselected: Zona de Restauración (ZR) and Cueva del Muerto (CM)located at Isla Larga, and at Isla Redonda, Plataforma Pavonas (PP)and Amarradero (AM) (Fig.1). A total of 189 coral fragments of threedifferent species w3e5 cm long were hand collected with SCUBA,Pocilopora damicornis (n ¼ 36), P. capitata (n ¼ 60) and P. verrucosa(n ¼ 93). In situ each sample was inspected and those fragmentswithout evidence of bleaching, dead tissue or a high amount ofsponge coverage were selected and re-attached within the samearea of collection using the plastic cable tie method (Edwards,2010) on both artificial and natural substrates.

Stable coral rubble was used as natural substrata (Fig. 2c) forall four study sites with depths of 3e8 m: Zona de Restauración(n ¼ 20), Cueva del Muerto (n ¼ 19), Amarradero (n ¼ 12), Pla-taforma Pavonas (n ¼ 21). Only at Zona de Restauración artificialunderwater structures were installed because fragments wereavailable in sufficient numbers for restoration. Artificial concretestructures (modules of 60 cm2) (n ¼ 10) had w12 steel-stackseach and were stabilized at 3e4 m depth (Fig. 2a). In both sub-strates each fragment was identified, measured and tagged. Coralgrowth progress was measured monthly (cm mo�1) during oneyear; using calipers (0.05 mm precision) noted maximum apicalheight growth distance measured from bottom to top of the

Fig. 2. Restoration approaches used (a) Initial coral fragments on artificial underwater structsize of coral fragments on natural substrate. (d) Final size after restoration on natural subs

fragment and maximum radial growth, referred as the longestdiameter perpendicular to the fragment height. Coral fragmentswere firmly adhered on the substrate were recorded as Attach-ment Rates; live fragments with a continuous growth over theentire experiment were recorded as Survivorship Rates and thosefragments which died in place during the study were recorded asMortality Rates.

Sea Water Temperature (SWT) was measured in situ every25 min during the counting process using HOBO� (Pendant) ther-mographs installed at both islands. Broken, missing and dead coralfragments were not used in the growth dataset.

2.3. Data analysis

Statistical analyses were calculated using Statistical 8� (Statsoft.Inc.) and Sigma Plot 11.0� (Systat software, Inc.) using a ¼ 0.05.Percentages of survivorship, mortality, and detachment rates werecalculated. All data sets were tested for normality (p < 0.05) andhomogeneity (p < 0.05) of variance. As data were not normallydistributed or homogenous, an analysis of variance on ranks(KruskaleWallis) was used to compare survivorship between spe-cies and sites. Growth and attachment rates were assessed withGeneral Linear Model (GLM) three-way ANOVA with fixed-effectsat substrate, species, and time levels, and two-way ANOVA atspecies and site levels. The change in growth and attachment ratesat substrate level were corroborated using ManneWhitney (U-test)to compare success of the substrate. KruskaleWallis was used totest difference of growth rates between sites and U-test was used toevaluate the difference in water temperature between Islands.Simple linear Pearson correlation (r) was used to correlate thegrowth variation with SWT.

ures. (b) Coral fragments after 12 months of restoration on artificial substrate. (c) Initialtrate.

Fig. 3. Fragment survivorship after one year period. (a) Pattern of survivorship ofdifferent coral species. (b) Comparison of survival between study sites (p < 0.05).

J.J.A. Tortolero-Langarica et al. / Ocean & Coastal Management 96 (2014) 12e19 15

3. Results

After one year 87% of the fragments survived on artificial and67% on natural substrate (Fig. 3). Resulting in 75% survivorship forall species, and important differences of survival between sites(H ¼ 9.306, p < 0.05), where Zona de Restauración recorded thehighest survivorship. The total losses were 20% by both detachment(14%) and mortality (6%). Detachment loss was 8% on natural and6% on artificial plots. Mortality associated with algal overgrowthwas observed during the first five months, showing mortality dif-ference between sites (H ¼ 8.539, p < 0.05), where 4% of the totaldeath occurred on fragments planted at 8 m depth on PlataformaPavonas, while minimal mortalities (�1%) were observed at Zonade Restauración (Fig. 3).

The annual data calculated at species level (Table 1) shows anincrease of 185% in height respect to initial size with maximumaccumulated growth of 6.38 � 2.11 cm yr�1 and minimum5.18 � 1.79 cm yr�1 (Fig. 4). Measurements of radial growthincreased 182%, with an annual growth from 5.63 � 1.73 cm yr�1 to4.80 � 1.41 cm yr�1, therefore showing no difference in height(F ¼ 1.278, p > 0.05) and radial measurement (F ¼ 1.057, p > 0.05)between species.

During the experiment neither natural nor artificial substratesreflected differences on growth between species either in height(F ¼ 0.109, p > 0.05) or radial growth (F ¼ 145, p > 0.05) (Table 1)with maximum accumulated growth values of 4.98 � 1.68 cm yr�1

in artificial underwater structures and 5.29 � 1.74 cm yr�1 in nat-ural substrata (Fig. 4). An important variation of growth was foundassociatedwith the effect of time (month) in both height (F¼ 2.876,p < 0.05) and radial growth (F ¼ 2.594, p < 0.05) independent fromsubstrates; July and November show differences (p < 0.05)compared with other months with a highest mean in height andradial measurements (Fig. 5). Comparisons between sites showCueva del Muerto attaining the highest mean height and radialgrowth 0.58 cm mo�1 and Amarradero the lowest (0.34 cm mo�1),both sites in the same Island. Our analyses shows that the differ-ence between sites does not influence height (H ¼ 3.433, p > 0.05)and diameter on coral growth (H ¼ 1.034, p > 0.05).

Attachment efficiency was 90% on artificial and 86% on naturalsubstrate, essentially no difference between species (F ¼ 1.941,p > 0.05): 93% for P. capitata, 90% for P. verrucosa and 89% forP. damicornis (Fig. 6). Attachment rates were between 4 and 6months, however different substrata resulted in different attach-ment speed (U ¼ 781.5, p < 0.001). Zona de Restauración had thehighest efficiency of attachment and Cueva del Muerto the lowest(Table 1), therefore showing the difference in study sites to have noeffect on attachment rate (F ¼ 0.432, p > 0.05).

Annual mean SWT at both Islands was (26.36 � 4.04 �C), with amarked difference between cold season (22.26 � 2.37 �C JanuaryeMay) and warm water season (29.54 � 1.28 �C JuneeNovember).Differences in mean annual SWT are associated to time (months)(H ¼ 21.431, p < 0.001) but not between Islands (U ¼ 127, p > 0.05).There was no correlation between coral growth and annual SWT(r ¼ 0.236, p > 0.05), however, a seasonal correlation was found,during the first five months (February to July) from cold to warmerwater temperatures there was shown to be a positive correlation(r ¼ 0.982, p < 0.05) (Fig. 5).

4. Discussion

Transplant methods are successful techniques previously usedto restore coral reef areas completely degraded (Guzmán, 1991;Rinkevich, 2005; Edwards and Gomez, 2007; Edwards, 2010;Lirman et al., 2010; Shaish et al., 2010; Young et al., 2012;Rinkevich, 2014), however, coral restoration is not commonly

employed at coral patches with coverage loss being evident but stillnot totally degraded (Reyes-Bonilla et al., 2002; Calderón-Aguileraand Reyes-Bonilla, 2006). The technique proposed has the advan-tage of not changing the physical and biological conditions of thesite and does not affect species succession (Shaish et al., 2010), andmost importantly, our restoration concept uses the natural frag-mentation of hermatypic branched, fast-growing corals such asPocillopora species. This rehabilitation tool is an accelerator to thenatural process of asexual reproduction (Highsmith,1982), which isassumed as the main reproduction mode in the region (Guzmán,1991), due to sexual reproduction (spawning or larvae release)has not been previously successful for the CMP (Carpizo-Ituarteet al., 2011).

Our results show high survivorship using both natural or arti-ficial substrate (Table 1, Fig. 3), and low mortality rate (6%)compared to different restoration techniques (Rinkevich, 2000,2005; 2008; Rojas et al., 2008; Edwards and Gomez, 2007;Edwards, 2010; Shaish et al., 2008, 2010; Levy et al., 2010; Liñán-Cabello et al., 2010; Gomez et al., 2011) using stable substrata in

Table 1Values recorded for Pocillopora fragments mean height (H) and radial growth (R), at different substrata: Natural and artificial. Sizes increase and attachment for differentspecies at different sites at Islas Marietas National Park, during 12 months of restoration.

Natural substrate Artificial substrate

n H(cm mo�1 �SD)

R(cm mo�1 �SD)

Attach(%)

H Increased(%)

R Increased(%)

n H(cm mo�1 �SD)

R(cm mo�1 �SD)

Attach(%)

H Increased(%)

R Increased(%)

SpeciesP. damicornis 8 0.53 � 0.35 0.28 � 0.35 75 199 157 21 0.52 � 0.27 0.45 � 0.16 99 201 194P. verrucosa 25 0.44 � 0.11 0.39 � 0.09 92 177 177 46 0.45 � 0.31 0.43 � 0.18 89 186 187P. capitata 15 0.28 � 0.30 0.44 � 0.30 87 172 182 33 0.44 � 0.16 0.47 � 0.19 99 175 192SiteZona de

Restauración17 0.48 � 0.24 0.39 � 0.24 100 193 178 100 0.43 � 0.29 0.464 � 0.27 96 187 191

Cueva del Muerto 12 0.58 � 0.13 0.51 � 0.25 75 186 193 e e e e e e

Amarradero 8 0.36 � 0.32 0.34 � 0.18 88 171 178 e e e e e e

PlataformaPavonas

11 0.38 � 0.18 0.34 � 0.14 82 172 163 e e e e e e

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both cases of natural or artificial substrate in order to provide thebest condition to attach the corals (Bothwell, 1982; Raymundoet al., 2007). The restoration technique in this study shows lowdetachment rates (14%). The losses were associated by extrinsiceffects such as poorly tied specimens or physical dislodgment as aresult produced naturally by waves, tides, currents and bio-erosion.

Fig. 4. Accumulated growth during 12 months. (a) Accumulated coral growth ofdifferent restoration techniques. (b) Comparison of accumulated coral growth betweendifferent species.

These losses were also reported for other restoration studies(Bowden-Kerby, 2001; Mbije et al., 2010; Garrison andWard, 2012).Efficiency attachment rates with the use of cable ties to bind frag-ments to the substrate, was similar compared with other attach-ment methods (Garrison and Ward, 2012; Forester et al., 2011).

Mortality was observed during the first fivemonths (February toJune). This has shown to be a common pattern (Muñoz-Chagin,1997; Yap et al., 1998; Lirman, 2000; Mbije et al., 2010; Shaishet al., 2010), due to high competition among associated groupssuch as coralline algae that may have continuous overgrowthduring the cold water season (Yap, 2004, 2009; Liñán-Cabello et al.,2010). However, this pattern changes as the SWT increases (>2 �C)and the tissue growth recovery becomes evident, which is aphysiologic pattern noticed for different hermatypic species (Clark,1997; Lirman, 2001; Rojas et al., 2008).

The mortality rate associated with coralline algae competitionaffects the survivorship of coral fragments differently betweensites. It is a well-known fact that the same species, depending on itslocation and life history, may respond differently to the environ-mental conditions (Somero, 2002; Middlebrook et al., 2008) andwill adapt or acclimatize to environmental change (Silverstein et al.,2012; Wooldridge, 2012). We have shown that differences inmortality rates, in the re-plantation technique, can be explained byfactors such as depth and temperature. At the Isla Redonda sites,plots were installed at 5e8 m depth and during the re-plantationtemperature drops until 15 �C, causing coral stress and enhancingalgae overgrowth and consequently, some fragments die,

Fig. 5. Relation between coral mean growth (bars) and monthly sea temperatures(circles), during 12 months of restoration at Islas Marietas.

Fig. 6. Attachment rates comparison among different sites and substrates. (a)Attachment rates between sites (p > 0.05). (b) Attachment rates between differentsubstrates. (*) differences among groups (p < 0.001).

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contributing to a 5% mortality rate. Unlike, Isla Larga plots wereinstalled at a shallower depth of 2e4 m and temperature rangesbetween 18 and 32 �C; as a result the combination of depth, lightand temperature resulted in lesser mortality rate of 1%. This dif-ference was not expected, as previous studies has demonstratedthat Pocillopora is acclimatized and had the ability to cope thedifferent micro-scale conditions (Rodríguez-Troncoso et al., 2010);however for practical purposes the data suggest Isla Larga as themost suitable site to enhance the coral restoration.

In the one year study, the specimens had a growth increase by 2-fold regardless of the substrata (Fig. 2). This is a higher growth ratereported for Pocillopora compared with other reports in the last 30years for this region (Guzmán,1991; Guzmán and Cortés,1993). Thespecies P. damicornis had the highest growth over the time span ofthe experiment but contrastingly, the slowest attachment rate onboth substrates; and despite P. verrucosa, does not having thehighest growth or the fastest attachment to the substrate, is thecoral species with the highest coverage and natural fragmentationin both islands. Therefore asexual recruit is presumed to be one ofthe successful reproductive strategies of P. verrucosa in the zone,and a possible reason for dominance and resilience (López-Pérezet al., 2007; Gomez et al., 2011).

On the other hand, the attachment rate on the different sub-strates used in this study show faster attachment on natural

substrate than on artificial (Fig. 6), this may be attributed to thesubstrata composition. Natural calcareous substrata develops thepresence of bacterial bio films which induces settlement andgrowth of many invertebrates (Wieczorek and Todd, 1997; Dahmset al., 2004; Dobretsov and Qian, 2006), also allows the presenceof calcareous coralline algae and other benthic organisms whoseacts as external chemical cues that promote positive coral recruit-ment and rapid attachment of coral fragments (Heyward and Negri,1999; Webter et al., 2004, 2011). So, the use of artificial structuresalthough as a general idea may increase the substrata available andcan be used as refugee by other associated organisms; however thismay change the physical condition of the area and as the artificialunderwater structures do not promote the fragments to attach, thecolony is not stable proving that this is not an effective or recom-mended method for coral restoration.

The use of small naturally fragmented corals resulted in a suit-able growth, fixation and survivorship on both substrates. The re-plantation technique resulted in affordable restoration because noextra timewas needed to go through the pre-acclimation process tore-attach, opposed to the transplantation processes used in coralnurseries (Shaish et al., 2010; Young et al., 2012; Rinkevich, 2014).One very important advantage is that no healthy corals are sacri-ficed from donor sites which may increase the chance of killing offhealthy donor colonies (Abelson, 2006). Another feature of the re-attachment is to avoid installation and maintenance costs thatinvolve floating nurseries (Levy et al., 2010; Young et al., 2012), plusthe concern of suitable transportation from the donor site (Muñoz-Chagin, 1997; Dodge et al., 1999; Omori and Fujiwara, 2004). Thisrestoration concept eliminates and solves relocation challengesthat transplantation may induce (Yap and Gomez, 1985; Yap et al.,1992; Baums, 2008), and may accelerate the reproduction strat-egy of asexual recruits using “corals of opportunity” (Monty et al.,2005; Edwards and Gomez, 2007). This promotes successfulrestoration in locations where natural fragmentation is present,and by not introducing corals from other localities, this in fact in-creases the chance of success by not changing the gene flow(Baums, 2008: Young et al., 2012).

The results of this study showed the major growth rate and themost attachment efficiency during the warmer season. Previousstudies show that temperature is one of the most important abioticfactors that regulate physiological activities such as growth, with apattern of high growth rate during warmwater temperatures and adecrease during cold temperatures (Dullo, 2005; Carricart-Ganivet,2011). At this point restoration actions have to consider the watertemperature as an important factor before start restoration pro-grams. Therefore, based on the results of this work it is recommendbegin during early summer that could be promote high survivor-ship, high growth and faster attachment rates with a successfulresults for restoration purposes.

5. Conclusions

Islas Marietas has a high social and biological value as it harborsone of the most important coral communities in the CentralMexican Pacific; it is also considered a hotspot tourist area wherethousands of visitors come each year. The Islands were declared aNational Park where government authorities and managers areapplying passive management measures such as legislation andregulation of standards to mitigate anthropogenic stress (CONANP,2007). However, since the inception of the IMNP, it has beenobserved that activities such as overfishing, diving, anchoring andopen boat access around the Islands plus the presence of naturalphenomena such as ENSO events have caused a continuousdecrease in coral coverage (Rodríguez-Troncoso and Cupul-Magaña, 2013). Active restoration management is urgent and will

J.J.A. Tortolero-Langarica et al. / Ocean & Coastal Management 96 (2014) 12e1918

be required to maintain the healthy coral coverage in order toconserve the high biodiversity associatedwith the coral population.The actions that we are proposing will help maintain the highecological value of the area and also the economic and social re-sources for the regional economy.

The present study shows that a reliable, low cost and short-termcoral restoration project can be performed through re-attachmentof coral fragments (Pocillopora spp.) on natural substrate, as wehave proven. This is a feasible and successful rehabilitation tool thatwe have proposed to be applied as long-term restoration programsfor IMNP and a promising technique in other locations in the Bayand we feel it can also be used in other degraded coral regionsworldwide. While these techniques should mitigate the coralcoverage loss, we also highly recommend applying other manage-ment strategies such as: public awareness, activity restrictions,educational workshops involving regional tourism agencies, localcommunities and stakeholders. These techniques andmanagementstrategies should increase the chances to regenerate the continuousloss of corals in response to unpredictable environment andanthropogenic impacts. It is also our belief that the restorationtechniques used in this study are the most suitable and practical inpreserving IMNP coral populations in the future and maintainingan important coral dispersal route between subpopulations overthe Eastern Tropical Pacific.

Acknowledgments

J.J.A.T.L work was supported by the doctoral fellowship CON-ACYT (No. 262538). The present work was supported by the project“Evaluación y monitoreo del efecto del Cambio Climático sobre lascomunidades coralinas del Pacífico Central Mexicano” (Project P/PIFI-2010-14MSU0010Z-10) to ACM and the project PROMEP220265 to APRT. Also, the authors thank the authorities from IslasMarietas National Park (CONANP) for the assistance and use of fa-cilities during the sampling and surveys, and to the “Instituto Tec-nológico of Bahía de Banderas” for their help with field operations.Finally, the authors would like to thank Kirstie L. Kaiser for theirvaluable comments to improve the manuscript.

References

Abelson, A., 2006. Artificial reefs versus coral transplantation as restoration tools formitigating coral reef deterioration: benefits, concerns and proposed guidelines.Bull. Mar. Sci. 78, 151e159.

Ammar, M.S.A., Amin, E.M., Gundacker, D., Mueller, W.E.G., 2000. One rationalstrategy for restoration of coral reefs: application of molecular biological toolsto select sites for rehabilitation by asexual recruits. Mar. Poll. Bull. 40, 618e627.

Baums, I.B., 2008. A restoration genetics guide for coral reef conservation. Mol. Ecol.17, 2796e2811.

Bothwell, A.M., 1982. Fragmentation, a means of asexual reproduction and dispersalin the coral genus Acropora (Scleractinia: Astocoeniida: Acroporidae): a pre-liminary report. In: 5th Int. Coral Reef Symp., pp. 137e144.

Bowden-Kerby, A., 2001. Low tech coral reef restoration methods modeled afternatural fragmentation process. Bull. Mar. Sci. 69, 915e931.

Calderón-Aguilera, L.E., Reyes-Bonilla, H., 2006. Can local oceanographic conditionsin the Mexican Pacific buffer the El Niño-Southern Oscillation effects on localreefs?. In: Proc. of 10th Int. Coral Reef Symp. Okinawa, Japan. June 28eJuly 2,2004, pp. 1138e1143.

Carpizo-Ituarte, E., Vizcaíno-Ochoa, V., Chi-Barragán, G., Tapia-Vázquez, O., Cupul-Magaña, A.L., Medina-Rosas, P., 2011. Evidence of sexual reproduction in thehermatypic corals Pocillopora damicornis, Porites panamensis, and Pavonagigantea in Banderas Bay, Mexican Pacific. Ciencias Mar. 37, 97e112.

Carricart-Gavinet, J.P., 2011. Coral skeletal extension rate: an environmental signalor a subject to inaccuracies? J. Exp. Mar. Biol. Ecol. 405, 73e79.

Carriquiry, J.D., Cupul-Magaña, A.L., Rodríguez-Zaragoza, F., Medina-Rosas, P., 2001.Coral bleaching and mortality in the Mexican Pacific during the 1997e98 ElNiño, and prediction from a remote sensing approach. Bull. Mar. Sci. 69, 237e249.

Carriquiry, J.D., Reyes-Bonilla, E.H., 1997. Community structure and geographic-distribution of the coral-reefs of Nayarit, Mexican Pacific. Ciencias Mar. 23,227e248.

Clark, S., Edwards, A.J., 1995. Coral transplantation as an aid to reef rehabilitation:evaluation of a case study in the Maldive Islands. Coral Reefs 14, 201e213.

Clark, T., 1997. Tissue regeneration rate of coral transplants in a wave exposedenvironment, Cape D’Aguilar, Hong Kong. In: Proc. 8th Int. Coral Reef Symp., vol.2, pp. 2069e2074.

CONANP, 2007. Programa de Conservación y Manejo del Parque Nacional IslasMarietas. Comisión Nacional de Áreas Naturales Protegidas, ISBN 978-968-817-851-5, 155 pp.

Cupul-Magaña, A., Calderón-Aguilera, L., 2008. Cold water bleaching at Islas Mar-ietas National Park, Nayarit, México. In: 15vo Congreso Nacional de Ocean-ografía,Veracruz, México.

da Silva, A.M., Young, C.C., Levitus, S., 1994. Atlas of Surface Marine Data 1994. In:Anomalies of Fresh Water Fluxes, vol. 4. NOAA Atlas NESDIS 9, 308 pp.

Dahms, H.U., Dobretsov, S., Qian, P.Y., 2004. The effect of bacterial and diatomsbiofilms on the attachment of the bryozoan Bugula neritina. J. Exp. Mar. Biol.Ecol. 313, 191e209.

Dight, I.J., Scherl, L.M., 1997. The International Coral reef Initiative (ICRI): globalpriorities for the conservation and management of coral reefs and the need forpartnerships. Proc. 8th Int. Coral Reef Symp. 1, 135e142.

Dobretsov, S., Qian, P.Y., 2006. Facilitation and inhibition of larval attachment of thebryozoan Bugula neritina in association with mono-species and multi-speciesbiofilms. J. Exp. Mar. Biol. Ecol. 333, 263e274.

Dodge, R.E., Anderegg, D., Fergen, R., Cook, P., 1999. Sewer Outfall Coral Trans-plantation Project. National Coral Reef Institute, Dania Beach, FL. Abstract: 80.

Dullo, W.C., 2005. Coral growth and reef growth: a brief review. Facies 51, 33e48.Edwards, A.J., Gomez, E.D., 2007. Reef restoration concepts and guidelines: making

sensible management choices in the face of uncertainty. In: St. Lucia, Australia:Coral Reef Targeted Research and Capacity Building for Management Program.

Edwards, A.J., 1998. Rehabilitation of coastal ecosystems. Mar. Poll. Bull. 37, 371e372.

Edwards, A.J., 2010. Reef rehabilitation manual. In: The Coral Reef Targeted Researchand capacity building for management program: Queensland, Australia, 166 p.

Fiedler, P.C., Talley, L.D., 2006. Hydrography of the eastern tropical Pacific: a review.Prog. Oceanogr. 69, 143e180.

Forrester, G.E., O’Connell-Rodwell, C., Baily, P., Forrester, L.M., Giovannini, S.,Harmon, L., Karis, R., Krumholz, J., Rodwell, T., Jarecki, L., 2011. Evaluatingmethods for transplanting endangered elkhorn corals in the Virgin Islands.Restor. Ecol. 19, 299e306.

Garrison, V.H., Ward, G., 2012. Transplantation of storm-generated coral fragmentsto enhance Caribbean coral reefs: a successful method but not a solution. Int. J.Trop. Biol. 60, 59e70.

Gaviño de la Torre, G., Uribe, Z., 1981. Distribución, población y época de la repro-ducción de las aves de las islas Tres Marietas, Jalisco, México. Inst. Biol. Univ.Autónoma Mex. Ser. Zool. 51, 505e524.

Glynn, P.W., Ault, P.S., 2000. A biogeographic analysis and review of the far easternPacific Coral Reef region. Coral reefs 19, 1e23.

Glynn, P.W., 2001. Eastern Pacific coral reef ecosystems. In: Seeliger, U., Kjerfve, B.(Eds.), Coastal Marine Ecosystems of Latin America, Ecol. Stud., vol. 144.Springer-Verlag Berlin Heidelberg, pp. 281e305.

Glynn, P.W., 2000. Effects of the 1997e98 El Niño Southern-oscillation on EasternPacific corals and coral reefs: an overview. Proc. 9th Int. Coral Reefs Symp. BaliIndones. 2, 1169e1174.

Gomez, E.D., Yap, H.T., Cabaitan, P.C., Dizon, R.M., 2011. Successful transplantation ofa fragmenting coral, Montipora digitata for reef rehabilitation. Coast. Manag. 39,556e574.

Guzmán, H.M., 1991. Restoration of coral reefs in Pacific Costa Rica. Conserv. Biol. 5,189e195.

Guzmán, H.M., Cortés, J., 1993. Arrecifes coralinos del Pacífico Oriental Tropical:Revisión y perspectivas. Rev. Biol. Trop. 41, 535e557.

Harriott, V.J., Fisk, D.A., 1988. Coral transplantation as a reef management option.Proc. 6th Int. Coral Reef Symp. 2, 375e379.

Heyward, A.J., Negri, A.P., 1999. Natural inducers for coral larval metamorphosis.Coral Reefs 18, 273e279.

Heyward, A.C., Smith, L.D., Rees, M., Field, S.N., 2002. Enhancement of coralrecruitment by in situ mass culture of coral larvae. Mar. Ecol. Prog. Ser. 230,113e118.

Highsmith, R.C., 1982. Reproduction by fragmentation in corals. Mar. Ecol. Prog. Ser.7, 207e226.

Hoegh-Guldberg, O., 2011. Coral reef ecosystems and anthropogenic climate change.Reg. Env. Change 11, 215eS227.

Hoegh-Guldberg, O., Mumby, P.J., Hooten, A.J., Steneck, R.S., Greenfield, P.,Gomez, E., Harvell, C.D., Sale, P.F., Edwards, A.J., Caldeira, K., Knowlton, N.,Eakin, C.M., Iglesias-Prieto, R., Muthiga, N., Bradbury, R.H., Dubi, A.,Hatziolos, M.E., 2007. Coral reefs under rapid climate change and ocean acidi-fication. Science 318, 1737e1742.

Jordan, W.R., Gilpin, M.E., Aber, J.D., 1987. Restoration Ecology: a Synthetic Approachto Ecological Research. Cambridge University Press, UK.

Kessler, W.S., 2006. The circulation of the Eastern tropical Pacific: a review. Prog.Oceanogr. 69, 181e217.

Levy, G., Shaish, L., Haim, A., Rinkevich, B., 2010. Mid-water rope nurseryetestingdesign and performance of a novel reef restoration instrument. Ecol. Eng. 36,560e569.

Liñán-Cabello, M.A., Flores-Ramírez, L.A., Laurel-Sandoval, M.A., Mendoza, E.,García, S., Olinda, S., Delgadillo-Nuño, M.A., 2010. Acclimation in Pocillopora spp.

J.J.A. Tortolero-Langarica et al. / Ocean & Coastal Management 96 (2014) 12e19 19

During a coral restoration program in Carrizales Bay, Colima, Mexico. Mar.Fresh. Behav. Physiol. 44 (1), 1e12.

Lirman, D., 2000. Fragmentation in the branching coral Acropora palmata(Lamarck): growth, survivorship, and reproduction of colonies and fragments.J. Exp. Mar. Biol. Ecol. 251, 41e57.

Lirman, D., 2001. Competition between macroalgae and corals: effects of herbivoreexclusion and increased algal biomass on coral survivorship and growth. CoralReefs. 19, 392e399.

Lirman, D., Thyberg, T., Herlan, J., Hill, C., Young-Lahiff, C., Schopmeyer, S.,Huntington, B., Santos, R., Drury, C., 2010. Propagation of the threatened stag-horn coral Acropora cervicornis: methods to minimize the impacts of fragmentcollection and maximize production. Coral Reefs 29, 729e735.

López-Pérez, R.A., Mora-Pérez, M.G., Leyte-Morales, G.E., 2007. Coral (Anthozoa:Scleractinia) recruitment at Bahía de Huatulco, Western México: implicationsfor coral community structure and dynamics. Pac. Sci., 61,355e61,369.

Mbije, N.E., Spanier, E., Rinkevich, B., 2010. Testing the first phase of the gardeningconcept as an applicable tool in restoring denuded reefs in Tanzania. Ecol. Eng.36, 713e721.

Middlebrook, R., Hoegh-Guldberg, O., Leggat, W., 2008. The effect of thermal historyon the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211,1050e1056.

Monty, J.A., Gilliam, D.S., Banks, K.W., Stout, D.K., Dodge, R.E., 2005. Corals ofopportunity, survivorship, and the use of coral nurseries in coral reefrestoration. In: Proc. 10th Int. Coral Reef Symp. Okinawa, Japan June 28eJuly2, 2004.

Muñoz-Chagin, R.F., 1997. Coral transplantation program in the Paraiso coral reef,Cozumel Island, Mexico. Proc. 8th Int. Coral Reef Symp. 2, 2075e2078.

Omori, M., Aota, T., Watanuki, A., Taniguchi, H., 2003. Development of coral reefrestoration method by mass culture, transportation and settlement of corallarvae. In: Toward the Desirable Future of Coral Reefs in Palau and WesternPacific, Proceedings. Palau Int. Coral Reef Center Publication, pp. 31e38. No.04-001.

Omori, M., Fujiwara, S., 2004. Manual for Restoration and Remediation of CoralReefs. Nature Conservation Bureau, Ministry of Environment, Japan, 84 pp.

Palacios-Hernández, E., Carrillo, L.E., Filonov, A., Brito-Castillo, L., Cabrera-Ramos, C.E., 2010. Seasonality and anomalies of surface temperature off thecoast of Nayarit, Mexico. Ocean Dyn. 60, 81e91.

Pandolfi, J.M., Connolly, S.R., Marshall, D.J., Cohen, A.L., 2011. Projecting coralreef futures under global warming and ocean acidification. Science 333,418e422.

Pantoja, D.A., Marinone, S.G., Parés-Sierra, A., Gómez-Valdivia, F., 2012. Numericalmodeling of seasonal and mesoscale hydrography and circulation in theMexican Central Pacific. Ciencias Mar. 38, 363e379.

Pennington, J.T., Mahoney, K.L., Kuwahara, V.S., Kolber, D.D., Calienes, R.,Chavez, F.P., 2006. Primary production in the Eastern tropical Pacific: a review.Prog. Oceanogr. 69, 285e317.

Petersen, D., Tollrian, R., 2001. Methods to enhance sexual recruitment for resto-ration of damaged reefs. Bull. Mar. Sci. 69, 989e1000.

Pickering, H., Whitmarsh, D., Jensen, A., 1998. Artificial reefs as a tool to aid reha-bilitation of coastal ecosystems: investigating the potential. Mar. Poll. Bull. 37,505e514.

Precht, W.F., Aronson, R.B., Swanson, D.W., 2002. Improving scientific decision-making in the restoration of ship-grounding sites on coral reefs. Bull. Mar.Sci. 69, 1001e1012.

Raymundo, L.J., Maypa, A.P., Gomez, E.D., 2007. Can dynamite blasted reefs recover?A novel, low-tech approach to stimulating natural recovery in fish and coralpopulations. Mar. Poll. Bull. 54, 1009e1019.

Reyes-Bonilla, H., Calderón-Aguilera, L.A., Cruz-Piñón, G., Medina Rosas, P., López-Pérez, R.A., Herrero-Perezrul, M.D., Leyte-Morales, G.E., Cupul-Magaña, A.L.,Carriquiry-Beltrán, J.D., 2005. Atlas de Corales Pétreos (Anthozoa:Scleractinia)del Pacıfico Mexicano. CICESE/CONABIO/CONACYT/UABCS/Universidad deGuadalajara/Universidad del Mar, México.

Reyes-Bonilla, H., Carriquiry, J.D., Morales, G.E., Cupul-Magaña, A.L., 2002. Effects ofthe 1997e99 El Niño and anti El Niño events on coral communities of the Pa-cific coast of México. Coral Reefs 21, 368e372.

Rinkevich, B., 2000. Steps towards evaluation of coral reef restoration by usingsmall branchs fragments. Mar. Biol. 136, 807e812.

Rinkevich, B., 2005. Conservation of coral reef through active restoration measures:recent approaches and last decade progress. Env. Sci. Tech. 39, 4333e4342.

Rinkevich, B., 2008. Management of coral reefs: we have gone wrong whenneglecting active reef restoration. Mar. Poll. Bull. 56, 1821e1824.

Rinkevich, B., 2014. Rebuilding coral reefs: does active reef restoration lead tosustainable reefs? Curr. Opin. Environ. Sustain. 7, 28e36.

Rodríguez-Troncoso, A.P., Carpizo-Ituarte, E., Cupul-Magaña, A.L., 2010. Differentialresponse to cold and warm water conditions in Pocillopora colonies from theCentral Mexican Pacific. J. Exp. Mar. Biol. Ecol. 391, 57e64.

Rodríguez-Troncoso, A.P., Cupul-Magaña, A.L., 2013. Efecto del blanqueamiento en lacobertura coralina del Parque Nacional Islas Marietas. In: 7mo Congreso Mex-icano y 1er Congreso Panamericano de Arrecifes Coralinos, Yucatán, México.

Rojas Jr., P.T., Raymundo, L.J., Myers, R.L., 2008. Coral transplants as rubble stabi-lizers: a technique to rehabilitate damaged reefs. In: Proc. of the 11th Int. CoralReef Symp. Ft. Lauderdale, Florida, 7e11 July 2008, Session number 24.

Sabater, M.G., Yap, H.T., 2002. Growth and survival of coral transplants with andwithout electrochemical deposition of CaCO3. J. Exp. Mar. Biol. Ecol. 272, 131e146.

Sale, P.F., 2008. Management of coral reefs: where we have gone wrong and whatwe can do about it. Mar. Pollut. Bull. 56, 805e809.

Schuhmacher, H., Van Treeck, P., Eisinger, M., Paster, M., 2000. Transplantation ofcoral fragments from ship groundings on electrochemically formed reefstructures. Proc. 9th Int. Coral Reef Symp. 2, 983e990.

Shaish, L., Levy, G., Gomez, E., Rinkevish, B., 2008. Fixed and suspended coralnurseries in the Philippines: establishing the first step in the "gardeningconcept" of reef restoration. J. Exp. Mar. Biol. Ecol 358, 86e97.

Shaish, L., Levy, G., Rinkevich, B., 2010. Employing a highly fragmented, weedy coralspecies in reef restoration. Ecolo. Eng. 38, 1424e1432.

Shea, D.J., Trenberth, K.E., Reynolds, R.W., 1992. A global monthly sea surfacetemperature climatology. J. Clim. 5, 987e1001.

Shuchumacher, H., van Treechk, P., Eisinger, M., Paster, M., 2002. Transplantation ofCoral Fragments From Ship Groundings on Electrochemically Formed ReefStructures. Proc. 9th Int. Coral Reefs Symp. Bali Indones vol. 2, 983e990.

Silverstein, R.N., Adrienne, M.S., Correa, A.C.B., 2012. Specificity is rarely absolute incoral-algal symbiosis: implications for coral response to climate change. Proc. R.Soc. B. http://dx.doi.org/10.1098/rspb.2012.0055.

Somero, G.M., 2002. Thermal physiology and vertical zonation of intertidal animals:optima, limits, and costs of living. Integ. Comp. Biol. 42, 780e789.

Treweek, J., 1999. Ecological Impact Assessment. Blackwell Science, Oxford, 351 p.Van Treeck, P., Schuhmacher, H., 1997. Initial survival of coral nubbins transplanted

by a new coral transplantation technology e options for reef rehabilitation. Mar.Ecol. Prog. Ser. 150, 287e292.

Wang, C., Fiedler, P.C., 2006. ENSO variability in the Eastern tropical Pacific: a re-view. Prog. Oceanogr. 69, 239e266.

Webster, N.S., Smith, L.D., Heyward, A.J., Watts, J.E.M., Webb, R.I., Blackall, L.L.,Negri, A.P., 2004. Metamorphosis of a scleractinian coral in response to mi-crobial biofilms. Appl. Environ. Microbiol. 70, 1213e1221.

Webster, N.S., Soo, R., Cobb, R., Negri, A.P., 2011. Elevated seawater temperaturecauses a microbial shift on crustose coralline algae with implications for therecruitment of coral larvae. ISME J. 5, 759e770.

Wieczorek, S.K., Todd, C.D., 1997. Inhibition and facilitation of bryozoan and ascidiansettlement by natural multi-species biofilms: effects of film age and the roles ofactive and passive larval attachment. Mar. Biol. 128, 463e473.

Wooldridge, S.A., 2012. A new conceptual model of coral biomineralization: hypoxiaas the physiological driver of skeletal extension. Biogeosci. Discuss. 9, 12627e12666.

Yap, H.T., Gomez, E.D., 1985. Growth of Acropora pulchra. III. Preliminary observa-tions on the effects of transplantation and sediment on the growth and survivalof transplants. Mar. Biol. 87, 203e209.

Yap, H.T., Alvarez, R.M., Custodio III, H.M., Dizon, R.M., 1998. Physiological andecological aspects of coral transplantation. J. Exp. Mar. Biol. Ecol. 229, 69e84.

Yap, H.T., Aliño, P.M., Gomez, E.D., 1992. Trends in growth and mortality of threecoral species (Anthozoa: Scleractinia), including effects of transplantation. Mar.Ecol. Prog. Ser. 83, 91e101.

Yap, H.T., 2004. Differential survival of coral transplants on various substrates underelevated water temperatures. Mar. Pollut. Bull. 49, 306e312.

Yap, H.T., 2009. Loca changes in community diversity after coral transplantation.Mar. Ecol. Prog. Ser 374, 33e41.

Young, C.N., Schopmeyer, S.A., Lirman, D., 2012. A review of reef restoration andcoral propagation using the threatened genus Acropora in the Caribbean andWestern Atlantic. Bull. Mar. Sci. 88, 1075e1098.