BIODIVERSITY AND ECOSYSTEM RESTORATION...and other dominant invaders, such as sauco (Cestrum auriculatum) and wandering jew (Tradescantia fluminensis; Figure 1). Of the 34 plots, 17

BIODIVERSITY AND ECOSYSTEM RESTORATION

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GALAPAGOS REPORT 2015 - 2016

Restoration of the blackberry-invaded Scalesia forest: Impacts on the vegetation, invertebrates, and birdsHeinke Jäger1, Sascha Buchholz2, Arno Cimadom3, Sabine Tebbich3, Jacqueline Rodríguez1, Denisse Barrera1, Anna Walentowitz4, Mareike Breuer2, Alonso Carrión5, Christian Sevilla5 and Charlotte Causton1

1Charles Darwin Foundation2Technische Universität Berlin, Germany 3University of Vienna, Austria4University of Greifswald, Germany5Galapagos National Park Directorate

Photo: © Steven Frank

The majority of studies on the impact of invasive plants have focused on single-species invasions despite the prevalence of co-occurring invasive species in many ecosystems that have the potential to interact (Kuebbing et al., 2013). Understanding the role of plant invaders in an ecosystem as well as interactions between and among species is important and can significantly affect the outcome of restoration programs (D’Antonio & Meyerson, 2002). A holistic approach toward restoration of the ecosystem is essential, though seldom undertaken (McAlpine et al., 2016). In the present study in the highlands of Santa Cruz Island in Galapagos, we addressed these shortcomings by investigating interactions among different invaders and by simultaneously assessing impacts of chemical blackberry control on the vegetation, invertebrates, and on bird numbers and breeding success in a forest dominated by the endemic Scalesia pedunculata tree at Los Gemelos.

The Scalesia forest, housing the highest number of plant and animal species in the highlands of Santa Cruz, has been drastically reduced by agricultural activities in the past and more recently, by invasive plants (Rentería & Buddenhagen, 2006). On Santa Cruz, about 100 ha remain, less than 1% of its original distribution, with the largest concentration at Los Gemelos (Mauchamp & Atkinson, 2011). One of the worst invasive plants at Los Gemelos is blackberry (Rubus niveus, Rosaceae), which grows vigorously and prevents recruitment of native species, thus changing the surrounding plant community (Rentería et al., 2012). Over more than ten years, the Galapagos National Park Directorate (GNPD) has successfully controlled blackberry at Los Gemelos by applying herbicides. However, there is concern that this intensive management has changed the structure of the forest, and is impacting the invertebrates and birds that live there (Cimadom et al., 2014). To evaluate this, we compared vegetation composition, insect abundance, bird numbers, and breeding success of two finch species, the green warbler-finch (Certhidea olivacea) and the small tree-finch (Camarhynchus parvulus), in two areas, one with a high density of blackberry and the other where the GNPD is actively controlling it.

Methods

To study the impacts of blackberry density and the chemical control of blackberry

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on the plant and animal communities, we defined two study areas at Los Gemelos, and, in 2014, established 34 permanent 10×10 m plots. All plots contained blackberry and other dominant invaders, such as sauco (Cestrum auriculatum) and wandering jew (Tradescantia fluminensis; Figure 1). Of the 34 plots, 17 were within an 8-ha area that was left untouched (referred to as the Reference Area), and 17 were within a 6-ha area where blackberry was controlled (Controlled Area). Invasive plants in the

Controlled Area were first cut down manually using a machete and after two months the regrowth was sprayed with herbicides (applying a mixture of glyphosate and Combo©). After another two months, re-sprouting invasive species were removed by a weed whacker and by hand. Monitoring of the vegetation, invertebrates, and birds was carried out once before control measures were applied, and then again in 2015 and 2016.

Figure 1. Study site at Los Gemelos, Santa Cruz: 17 permanent plots in the Reference Area (lower left corner) and 17 plots in the Controlled Area where blackberry was chemically controlled (upper right corner).

Results and Discussion

Plants

Control measures were successful in reducing blackberry cover; however, blackberry cover also decreased, though to a lesser degree, in the Reference Area over the same period (Figure 2). This may be because blackberry goes through a natural die-back cycle and then recovers again (H Jäger, pers. observ.). Wandering jew and sauco cover increased in the Controlled Area and it is probable that the presence of these species suppresses germination and/or growth of blackberry. Because of this, it might be beneficial to leave them in areas that they have invaded. Although these are also invasive species with a potential negative impact on the surrounding vegetation, they are less harmful than blackberry and their removal seems to

facilitate the germination and/or growth of blackberry.

Percent cover of the non-dominant plant species (herbs, grasses, shrubs, and trees) also increased after chemical control of blackberry (Figure 2), which could be an indication of recovery. However, the number of non-dominant introduced species and species of unknown origin increased after control actions were carried out (Figure 3 A, D) and could have accounted for a higher total plant cover. At the same time, total number of species remained roughly the same, whereas the total number of endemic species slightly decreased (Figure 3 B, C). This trend was not observed in the Reference Area (Figure 3 A-D) indicating that disturbance caused by the control measures might have facilitated the expansion of invasive species and establishment of other introduced species, as was also shown in the case of

Los Gemelos

Controlled Area

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Figure 2. Percent cover of the dominant invasive species sauco (Ces_aur), blackberry (Rub_niv), wandering jew (Tra_flu), and the endemic Scalesia pedunculata (Sca_ped), and of the non-dominant, remaining vegetation (non_dom) at the study sites (N=17 each for the Controlled and Reference Areas).

Figure 3. Total number of non-dominant plant species at the two study areas: A – Questionable native species (NaQ; origin unknown, could be native or introduced); B - native species; C - endemic species, and D - introduced species (N=17 each for the Controlled and Reference Areas).

quinine control (Jäger et al., 2009; Jäger & Kowarik, 2010). Future monitoring is needed to show whether this is an ephemeral phenomenon or not.

Percent cover of Scalesia pedunculata in the Reference Area decreased by a third over the monitoring period (Figure 2 A), which could be due to tree mortality. Over the course of two years, 71 out of 200 (35.5%) trees died in the Reference Area. The reason for this is not clear but could have been caused by strong winds that occurred in the highlands

of Santa Cruz during February 2016. No new seedlings were found in this area. During the same time, 47 out of 255 (18.4%) trees died in the Controlled Area; however, the chemical control of blackberry had a spectacular effect on the regeneration of Scalesia pedunculata. Only five months after the last herbicide application by the GNPD, up to 280 Scalesia seedlings per plot were found at the Controlled Area where there had been none during our first monitoring. This was reflected by an increase in Scalesia cover in the Controlled Area (Figure 2 B).

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We also determined that the threshold of blackberry cover that the resident plant species (native and endemic) can tolerate, and under which they can still thrive, is about 60%. These results confirm those of Rentería et al. (2012), who also determined a 60% blackberry cover as (barely) tolerable for the persistence of the resident plant species in the understory. While this percentage is far from ideal, it can serve as a guideline for management actions.

Invertebrates Around 16,184 specimens were collected from Malaise traps and 766 from Pitfall traps set out in the study areas.

Analyses at species level are pending. At this stage, it is difficult to reach conclusions about the dynamics of invertebrates in both study areas. Preliminary data on spider abundance (Araneae) showed similar trends in the Reference Area and Controlled Area (Figure 4), suggesting that climate might influence invertebrate numbers at both sites. However, this does not explain the difference in abundance between the two study areas prior to and after control efforts. Further analyses and continued monitoring are needed to determine whether management efforts have affected invertebrate diversity and abundance.

Figure 4. Total number of spiders caught in Malaise traps (results shown are sums of individuals caught in two Malaise traps placed in each area for four weeks), and in 51 Pitfall traps (three traps per plot placed in each area).

Figure 5. Percentage of successful nests (at least one fledgling per nest) of green warbler-finches and small tree-finches.

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The breeding success of the green warbler-finch and small tree-finch did not differ significantly between the two areas in any of the three years (Figure 5). The comparison within

area before and after the control measures was influenced by drought conditions in 2015. Breeding success in this year was extremely low for both species in both areas. The overall very low breeding success may have masked the short-term effect of the mechanical and chemical control

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that had been observed in previous years (Cimadom et al., 2014). In 2016, which was the second breeding season after the control measures, the breeding success of the green warbler-finch was lower in the Controlled Area than in the Reference Area, indicating a negative effect of habitat management. Breeding success of the small tree-finch was extremely low in both areas throughout the study.

We found no significant detrimental (negative) effect of invasive plant management on bird numbers. Bird counts showed a slight increase of singing males per point in 2015 and 2016 compared to 2014 in most species in both areas. The only pronounced change was an increase in the number of small ground-finches in the Controlled Area in 2015, right after the implementation of control measures. This species seems to move into the open areas created by the removal of the understory.

Conclusions and Recommendations

Long-term monitoring will reveal more about how animal and plant communities respond to blackberry removal. In the meantime, preliminary results indicate that methods to control blackberry are effective and that blackberry regeneration can be prevented by other invasive, but less detrimental, plants. Regeneration of Scalesia pedunculata was only possible in blackberry-controlled areas and was very high, suggesting that interventions to control this invasive plant are needed. However, the continuous germination of blackberry seeds in the Controlled Area requires follow-up removal of blackberry seedlings for several years after intervention.

To ensure the continued success of this control program, the following management actions are recommended:

1. Maintain a long-term monitoring program to evaluate blackberry control methods and results.

2. Do not control sauco and wandering jew in the protected areas as their presence tends to help suppress blackberry.

3. Maintain the cover of blackberry at 60% or less to ensure survival of surrounding vegetation.

4. Continuously remove blackberry seedlings by hand-pulling from areas that have been controlled, as blackberry regenerates vigorously from seeds.

5. Analyze herbicide residuals in soil and water samples at Los Gemelos to assess contamination.

Acknowledgements

We would like to acknowledge the financial support by Galapagos Conservancy and Keidanren Nature Conservation Fund to carry out the vegetation and invertebrate monitoring. We are also very grateful for the hard work of the GNPD park rangers who made this study possible. The bird monitoring was supported by a FWF-grant from the Austrian Government. Furthermore, we would like to thank the numerous local, national, and international field assistants for their help in data collection and processing.

ReferencesCimadom A, A Ulloa, P Meidl, M Zöttl, E Zöttl, B Fessl, E Nemeth, M Dvorak, F Cunninghame & S Tebbich. 2014. Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin’s Finches. PLoS ONE 9, e107518, doi:10.1371/journal.pone.0107518.

D’Antonio CM & LA Meyerson. 2002. Exotic plant species as problems and solutions in ecological restoration: a synthesis. Restoration Ecology 10:703-713.

Jäger H, I Kowarik & A Tye. 2009. Destruction without extinction: Long-term impacts of an invasive tree species on Galapagos highland vegetation. Journal of Ecology 97:1252-1263.

Jäger H & I Kowarik. 2010. Resilience of a native plant community following manual control of the invasive Cinchona pubescens in Galápagos. Restoration Ecology 18:103-112.

Kuebbing SE, MA Núñez & D Simberloff. 2013. Current mismatch between research and conservation efforts: The need to study co-occurring invasive plant species. Biological Conservation 160:121-129.

Mauchamp A & R Atkinson. 2011. Rapid, recent and irreversible habitat loss: Scalesia forest on the Galapagos Islands. Galapagos Report 2011-2012. GNPS, GCREG, CDF and GC. Puerto Ayora, Galapagos, Ecuador.

McAlpine C, CP Catterall, R Mac Nally, D Lindenmayer, JL Reid, KD Holl, AF Bennett, RK Runting, K Wilson, RJ Hobbs, L Seabrook, S Cunningham, A Moilanen, M Maron, L Shoo, I Lunt, P Vesk, L Rumpff, TG Martin, J Thomson & H Possingham. 2016. Integrating plant- and animal-based perspectives for more effective restoration of biodiversity. Frontiers in Ecology and Environment 14:37-45.

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Rentería JL & CE Buddenhagen. 2006. Invasive plants in the Scalesia pedunculata forest at Los Gemelos, Santa Cruz, Galapagos. Noticias de Galápagos - Galapagos Research 64:31-35.

Rentería JL, MR Gardener, FD Panetta, R Atkinson & MJ Crawley. 2012. Possible impacts of the invasive plant Rubus niveus on the native vegetation of the Scalesia forest in the Galapagos Islands. PLoS One 7(10). Doi:10.1371/journal.pone.0048106.

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The avifauna of many oceanic archipelagos has been seriously affected by the arrival of introduced predators and disease agents, which, combined with habitat alteration, has led to declines or extinctions for many species (Steadman, 2006). Invasive species can cause rapid extinction of island populations because of few natural enemies (enemy release hypothesis; Maron & Vilà, 2001), and because they often have traits novel to the native species (novel weapons hypothesis; Callaway & Aschehoug, 2000).

Galapagos landbirds1 face similar threats (Wikelski et al., 2004; Parker et al., 2006; Wiedenfeld & Jimenez Uzcátegui, 2008). A significant amount of genetic diversity of Darwin’s finches has disappeared over the last 100 years (Petren et al., 2010), and several populations or subspecies have experienced substantial declines or are extinct on inhabited islands (Grant et al., 2005; Dvorak et al., 2012; Merlen, 2013). Until recently, little was known about the abundance of most Galapagos landbird species (Cunninghame et al., 2012); most research focused on uninhabited islands or evolutionary questions.

A recent assessment (IUCN, 2016) identifies 14 of the 28 small native or endemic landbirds (passerines, cuckoos, and doves) as threatened with extinction (Table 1). The updated IUCN Red List takes into account recent genetic studies and includes a change to species for the two former sub-species of the vermilion flycatcher (Carmi et al., 2016), the splitting of the large cactus-finch into two species (Farrington et al., 2014, Lamichhaney et al., 2015), and the splitting of the highland sharp-beaked ground-finch from the morphologically and ecologically (Grant et al., 2000) highly distinctive lowland populations (Farrington et al., 2014, Lamichhaney et al., 2015). A group that is still in need of revision is the tree finches Camarhynchus (Nemeth & Dvorak, unpubl. data), which includes the subspecies of the woodpecker finch from San Cristóbal (C. pallidus striatipectus, Figure 1).

Galapagos landbirds (passerines, cuckoos, and doves): Status, threats, and knowledge gapsBirgit Fessl1, David Anchundia1, Jorge Carrión2, Arno Cimadom3, Javier Cotin1, Francesca Cunninghame1, Michael Dvorak4, Denis Mosquera1, Erwin Nemeth4, Christian Sevilla2, Sabine Tebbich3, Beate Wendelin5 and Charlotte Causton1

1Charles Darwin Foundation2Galapagos National Park Directorate3Universiy of Vienna, Austria4 BirdLife Austria5 Frohnatur Austria

Photo: © David Anchundia

1 Scientific species names are given in Table 1; subspecies names are indicated in the text when needed.

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Figure 1. Differences in plumage between woodpecker finches from San Cristóbal (left) and Santa Cruz (right). Photo: M. Dvorak

Table 1. Threat status, distribution, relative abundance, and known Philornis downsi infestation for passeriformes, cuckoos, and doves in the Galapagos Islands. Knowledge gaps are indicated. Island extinctions are highlighted in orange, with important notes on population status highlighted in yellow. Species that can be monitored by residents, tourists, naturalist guides, and park rangers are identified with CS (Citizen Science).

In response to the declines in some landbird populations, the Charles Darwin Foundation (CDF) and the Galapagos National Park Directorate (GNPD), in collaboration with a group of ornithologists, developed a landbird conservation plan (Cunninghame et al., 2012). This plan aims to clarify the conservation status of landbirds on all islands (Tables 1 & 2), and develop management actions. Based on this information and follow-up monitoring work,

it will be possible to detect and respond to population changes. Here we provide an overview of the surveys conducted on the four inhabited islands and Santiago within the past six years, and identify factors that may be responsible for the decline of some species.

1 For Latin names we follow the South American Classification Committee except for the Vermilion flycatcher, which we consider a species in this paper (see Carmi et al., 2016).

2 IUCN threat categories from low to high threat status: Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), Critically Endangered (CR), Extinct (EX).

3 E= endemic species, N = native species, I = introduced species

Species name1IUCN-status2

Origin (E, N, I)3

Number of subspecies [ ]

Distribution and habitat type Known host for Philornis downsi

Islands with knowledge gaps

Options for citizen science (CS)

Small ground-finch Geospiza fuliginosa LC, stable, E

Common; on all main islands except Genovesa, Darwin, and Wolf.

All vegetation zones.Host of P. downsi.

None

Medium ground-finch Geospiza fortis LC, stable, E

Common; on all main islands except Genovesa, Española, Darwin, and Wolf.

Host of P. downsi.

At risk on Floreana, more studies needed

Large ground-finch Geospiza magnirostris LC, stable, E

Present on all islands except Española and Darwin. All islands; habitat prefer-ence not completely

understood; very patchy distribution on Santa Cruz

and possibly all other larger islands. Difficult to get

valuable density data with currently applied counting

methods. CS

Extinct on Floreana and San Cristóbal.

Lowlands.Host of P. downsi.

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Sharp-beaked ground-finchA

Geospiza difficilisLC, stable, E

Occurs in highland forest on Santiago, Fernandina and Pinta.

Pinta, Fernandina. CSExtinct on Santa Cruz, San Cristóbal, Floreana, and probably Isabela.

Studies on P. downsi missing.

Genovesa ground-finchA

Geospiza acutirostrisVU (classified as a species in

2016), stable, EGenovesa.

P. downsi not reported for Genovesa. Genovesa

Vampire ground-finchA

Geospiza septentrionalisVU (classified as a species in

2016), stable, EDarwin and Wolf.

P. downsi not reported for Darwin and Wolf.

Common cactus-finchGeospiza scandens LC, stable, E [4]

Present on all main islands except Fernandina, Española, Genovesa, Darwin, and Wolf.

Floreana, San Cristóbal, Isabela, Santiago. CS

Extinct on Pinzón.

Apparently very rare on San Cristóbal (few records during surveys).

Arid zone with cacti.Host of P. downsi.

Española ground-finchB Geospiza conirostris

VU ( classified as a species in 2016), stable, E

Believed to be common on Española. Arid zone with cacti.

P. downsi not reported for Española.Española

Genovesa cactus-finchB

Geospiza propinguaVU (classified as a species

in 2016), stable, EBelieved to be common on Genovesa. P. downsi not reported for Genovesa. Genovesa

Vegetarian finch Platyspiza crassirostris LC, stable, E

Present on all main islands except Santa Fe, Genovesa, Española, Darwin, and Wolf.

All uninhabited islands except Santiago highlands. Little is known about this

species; an ecological study would be worthwhile.

Possibly extinct on Floreana.

Arid and transition zones.Host of P. downsi.

Small tree-finchCamarhynchus parvulus LC, stable, E [2]

Present on all main islands except Marchena, Genovesa, Española, Darwin, and Wolf.Highlands; lower densities in lowlands.

Host of P. downsi.

All uninhabited islands except Santiago highlands.

Medium tree-finch Camarhynchus pauper

CR (since 2009), decreasing, E

Floreana; the population is larger than previously thought and seems stable but breeding success is

possibly low.Long-term study ongoing

(S Kleindorfer, Flinders University, Australia).Highland forest.

Host of P. downsi.

Large tree-finch Camarhynchus psittacula

VU (since 2015), decreasing, E [3]

Present on all main islands except San Cristóbal, Española, Genovesa, Darwin, and Wolf.

Fernandina, Isabela volcanoes, Pinta, Marchena,

Rábida, Santiago, Pinzón, and Santa Fe.

Genetic studies on differences among islands

necessary to evaluate status of currently described

subspecies.

Extinct (if ever permanently present) on Floreana.

Low densities on Santa Cruz and Sierra Negra Volcano, Isabela.

No quantitative data from all other islands and possibly severely threatened.

Highland and transition forest.Host of P. downsi.

Woodpecker finch Camarhynchus pallidus

VU (since 2015), decreasing, E [3]

Present on Isabela, Santiago, Santa Cruz and San Cristóbal. Genetic, morphological,

and ecological studies on differences between islands in progress (E Nemeth & M Dvorak, BirdLife Austria). Confirmation of doubtful

island occurrences.

Possibly occurring (single specimens or unconfirmed sight records) on Pinta, Fernandina,

Pinzón, Rábida, and Santa Fe.

Highlands; very low densities in arid zones.Host of P. downsi.

A,B, Formerly considered as one species; changed due to genetic evidence shown by Farrington et al., 2014, Lamichhaney et al., 2015. See as well Proposal roster 676 published by the South American Classification Committee.

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* Species that cannot be assessed properly with the point count method because of their rarity or special habitat requirements.

Mangrove finch Camarhynchus heliobates

CR (since 2000), decreasing, E

Isabela and Fernandina. Some known hybridization with the woodpecker finch.

This species is currently under intensive management by the Mangrove Finch Project (GNPD

& CDF). Continuous funding and support needed to keep the

species viable.

Mangrove forest. At the moment only breeding population north of Tagus Cove.

Host of P. downsi.

Green warbler-finch Certhidea olivacea

LC (classified as a species in 2016), stable, E

Isabela, Santa Cruz, Fernandina, Santiago, Pinzón, and Rábida.

Highland zones into transition zone.Host of P. downsi.

Fernandina, Pinzón, Rábida, and Isabela except Sierra Negra.

Gray warbler-finch Certhidea fusca

LC (classified as a species in 2016), stable E [6]

San Cristóbal, Marchena, Española, Pinta, Santa Fe, and Genovesa. Marchena, Pinta, Santa Fe,

Española, and Genovesa.Clarify taxonomic status of birds

from San Cristóbal.

Extinct on Floreana.

Inhabits dry zone on most islands; in San Cristóbal known from transition zone up into the highlands.


Yellow warbler Setophaga petechia

LC, stable, N (endemic subspecies for Galapa-gos and Cocos Island)

All main islands and all habitat types.Host of P. downsi.


Little vermilion flycatcher* Pyrocephalus nanus

VU (classified as a species in 2016), decreasing, E

All main islands except Genovesa, Española, and Baltra.

All islands. CS. Nest success study at El Cura,

Sierra Negra, Isabela in progress (CDF).

Probably extinct from Floreana.

Rare on Santa Cruz and Santiago.

On some islands only in highlands and transition zones; on small islands also known

from the lowlands.Host of P. downsi.

Least vermilion flycatcherPyrocephalus dubius

EX (classified as a species in 2016) San Cristóbal; last seen in 2008.

Recent surveys (2015-2016) unsuccessful in finding species. Searches in very remote areas

needed to confirm status.

Galapagos flycatcherMyiarchus magnirostris LC, stable, E

Present on all islands except Genovesa, Darwin, and Wolf.

Lower numbers in highlands.Host of P. downsi.


Galapagos mockingbird Mimus parvulus LC, stable, E [6]

Present on all main islands without island-specific species.

More common in lowlands. Lower numbers in highlands.

Host of P. downsi.

Fernandina, Marchena, and Santa Fe. CS.

Floreana mockingbirdMimus trifasciatus CR (since 2008), E

Extinct on Floreana. This species is currently under care of the Floreana Mocking-

bird Project (GNPD and Massey University, New Zealand). No

management needed so far as populations appear stable

(L. Ortiz-Catedral, pers. comm.).

Small remnant populations on two islets (Champion & Gardner) close to Floreana.

Host of P. downsi.

Española mockingbird Mimus macdonaldi VU (since 2008), E Española.

P. downsi not reported for Española.

No information on status; systematic population survey

necessary.

San Cristóbal mockingbird Coccyzus melacoryphus EN (since 2006), E

San Cristóbal.Common in all habitats.

Host of P. downsi.

Arid zone on San Cristóbal, especially outside easily

accessible sites. CS.

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* Species that cannot be assessed properly with the point count method because of their rarity or special habitat requirements.

Dark-billed cuckoo Coccyzus melacoryphus LC, stable, N All main islands and all habitat types.

Host of P. downsi.

All uninhabited islands. Little to nothing is known

about this species (including genetics).

Calling activity highly variable between years, therefore difficult to obtain reliable population estimates. CS.

Galapagos dove Zenaida galapagensis LC, stable, E [2]

All main islands and all habitat types. All uninhabited islands. Has become very rare on inhabited islands, thus special attention

needed to look at factors causing decline. CS.

Very rare on San Cristóbal, Floreana and patchy distribution on Santa Cruz.


Galapagos martin* Progne modesta EN (since 2008), E

Present in low numbers on all islands. Unobserved from Marchena, Genovesa, Pinta, Darwin, and Wolf.

All islands. This species needs a special

program to be properly assessed. CS.

Needs cliffs for nesting.


Smooth-billed ani Crotophaga ani LC, stable, I

Present on all main islands. Status on Fernandina unknown.

Eradicated from Marchena. All habitat types.Host of P. downsi.

All islands. Reports from all islands other

than inhabited ones needed to assess distribution. CS.

Bird population surveys

For the first time we have baseline data for all passerine species and most other landbirds from San Cristóbal, Floreana, Santa Cruz, the highlands of Santiago, and Sierra Negra volcano on Isabela (Table 2).

San Cristóbal

This is the oldest island of the Archipelago and the only one with running fresh water. Permanent human settlements began in 1837; current population is estimated at 7500 residents (INEC, 2010). While natural vegetation remains in the lowlands, there is little native vegetation left in the humid highland zone as a result of intensive agriculture (Watson et al., 2010). Of the 11 small landbird species that were collected and mentioned by Swarth (1931), the vermilion flycatcher (last seen in 2008) was missing in the recent survey; the Galapagos dove and the common cactus-finch were very rare. The latter two might be more common in unsurveyed parts of the arid zone.

The introduced smooth-billed ani, encountered in all habitat types, was rare in the arid zone. The population of the endangered San Cristóbal mockingbird, encountered in all vegetation zones, is several times larger (10-15,000 breeding pairs) than the 8000 individuals estimated in 2005 (IUCN, 2016).

Floreana

Pirates and whalers were impacting the flora and fauna before the first human settlement in 1832. Furthermore, the effects of introduced mammals (e.g., cattle, goats, donkeys, and cats) were more severe on Floreana than on other Galapagos Islands (Steadman, 1986), probably leading to the disappearance of the Floreana mockingbird (Mimus trifasciatus) now confined to two small satellite islands (Steadman, 1986; Jiménez-Uzcátegui et al., 2011), and the sharp-beaked ground-finch, now extinct (Sulloway, 1982). Today, the human population numbers about 150. Floreana is home to one of the largest preserved endemic highland Scalesia forests in the Archipelago. Nevertheless, during our counts we recorded no vermilion flycatchers, large tree-finches, gray warbler-finches (subspecies Certhidea fusca ridwayi), or vegetarian finches. The first three species were already suspected to be extinct (Grant et al., 2005; Merlen, 2013; Kleindorfer et al., 2014a), while the absence of the vegetarian finch, formerly common (47 specimens collected in 1905/06; Swarth, 1931), was unexpected. The most recent records of vegetarian finches are from 1962, by R. Bowman (www.macaulay-library.org), 2004 (Grant et al., 2005), and 2008 (O’Connor et al., 2010c). The Galapagos dove was only found at two sites in the highlands and one site in the lowlands; it may still exist in remote areas of the arid zone. Lastly, the medium ground-finch and the common cactus-finch, both lowland species, seem to have declined considerably compared to the high numbers collected in 1905/06 (Swarth, 1931), and may be at risk of disappearing from Floreana.

Sources: Harris, 1973; Wiedenfeld, 2006; IUCN, 2016; own unpublished data

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On the other hand, our population estimate of 3900-4700 territories for the medium tree-finch is considerably higher than the previous estimate of 1620 males (O’Connor et al., 2010a). Our monitoring data provide the most accurate delimitation of the breeding range of this species, showing that it is not confined to the Scalesia forest but

the majority of the breeding population inhabits farmland and abandoned farmland, now part of the Galapagos National Park, characterized by a mixture of introduced and native vegetation with high trees (mainly Cedrela odorata) (Dvorak et al., unpubl. data).

Table 2. Avian survey/baseline data available for each island including status of Philornis downsi and recommended monitoring activities. Blue indicates sites with existing baseline data and suggested regular monitoring; highest priority baseline data collection sites highlighted in orange and second highest priority baseline collection sites in yellow.

Island Size (km2) Existing survey data / Status P. downsi Recommended locations and frequency of monitoring program

Isabela 4588Sierra Negra, 2015 (CDF/GNPD landbird project),

Playa Tortuga Negra since 2006, Wolf Volcano 2015 (landbird project) / P. downsi present

Alcedo, Cerro Azul, Darwin, Wolf, and lowlands including Pto. Villamil, Sierra Negra

Santa Cruz 986Multiple years since 1996 (Dvorak et al., 2012), last

comprehensive survey 2014 (Dvorak, Nemeth & Wendelin) / P. downsi present

Northern arid zone

Scalesia: every breeding season Other habitat zones: every 3-5 years

Fernandina 642 P. downsi presentHighlands: important for assessment of the sharp-beaked ground-finch and other tree

finches

Santiago 585 Highlands in 2016(CDF/GNPD landbird project) / P. downsi present

Lowlands and transition zone forest

Highlands should be repeated in 3-5 years

San Cristóbal 558 Lowlands 2010 (Dvorak & Nemeth), island-wide 2015 (landbird project) / P. downsi present

Additional sites in the dry zone and very remote areas for the vermilion flycatcher

(in cooperation with GNPD)

Highlands: every 3-5 years

Floreana 1732004, 2008, 2011 (highlands, Kleindorfer et al.); 2010 & 2014 (highlands, Dvorak & Nemeth); 2015 & 2016 (island-wide, landbird project) / P. downsi present

Repeat survey in 3-5 years

Marchena 130 P. downsi present All island: important for the large tree-finch

Española 60 2010 (CDF) / P. downsi absent

Island without any identified threats or endangered species (other than Española

mockingbird). However, recent authorization of day-tours makes baseline

monitoring fundamental.

Pinta 60 2014 (Keller et al.) / P. downsi presentImportant for assessment of the sharp-beaked

ground-finch, woodpecker finch, and large tree-finch

Baltra 27 2014 (UCSC-CCAL, outside breeding season) / P. downsi present

Lowest priority; island with cat eradication, no endangered species; assessment of

Galapagos dove density of importance for possible re-population of Santa Cruz

Santa Fe 24 P. downsi present All island, important for the large tree-finch

Pinzón 18 2010, 2012, 2014 (UCSC-CCAL, outside breeding season) / P. downsi present Important for baseline data after rat eradication

Genovesa 14 1973, 1978-1988 (Grant et al.); 2014 (Keller et al.) / P. downsi absent

Island without any identified threats; assessment of sharp-beaked ground-finch, large ground-finch. and large cactus-finch

Rábida 5 2010, 2012, 2014 (UCSC-CCAL, outside breeding season) / P. downsi present Important for baseline data after rat eradication

Sources: Wiedenfeld et al., 2007, Fessl et al., 2010a; O’Connor et al., 2010c; Dvorak et al., 2012; Luzuriaga et al., 2012

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The smooth-billed ani is common in all ecological zones.

Agricultural and fern zone of Sierra Negra Volcano, Isabela

The forested highlands (agricultural and park area) are covered by secondary vegetation, mainly guava (Psidium guajava) and Ecuadorian walnut (Juglans neotropica). Our bird surveys in 2015 provide the first estimates of landbird distribution and abundance for this area. The small ground-finch, small tree-finch, green warbler-finch, woodpecker finch, and yellow warbler are common, while the large tree-finch is restricted to areas with high trees only. The vermilion flycatcher is widespread and common in El Cura at an elevation between 550 and 1050 m (D Mosquera, unpubl. data). They seem to prefer older guava forests or stands where farmers have removed the dense understory. Density is lower at decreasing elevations and may be associated with clearing of guava stands, deserving special attention in the future.

Santiago

This currently uninhabited island was historically a source of fresh water, wood, and tortoises for buccaneers and whalers. In the 1920s and 1960s, salt was extracted commercially. Goats, pigs, and donkeys were released in the early 1800s and changed the highland zone considerably, though vegetation is recovering since their successful eradication (Cruz et al., 2005; Carrión et al., 2007; Cruz et al., 2009). All landbird species noted by Swarth (1931) were recorded in our survey in 2016, which focused on the highlands. The sharp-beaked ground-finch was widely distributed, but occurred only in comparatively low densities. The vermilion flycatcher and large tree-finch were encountered only at one site each in transition forest dominated by Galapagos guava (Psidium galapageium). A thorough search is necessary to further clarify the status of these species. The island has a healthy population of Galapagos doves, with birds observed in all habitat types. They were frequently seen digging into the abundant tortoise dung searching for food.

Santa Cruz

Since the 1980s, Santa Cruz Island, settled in 1920, has had the highest human population (currently >15,000) and the highest population growth (Epler, 2007; INEC, 2006; INEC, 2010). The endemic Scalesia forest is reduced to 1% of its former extent (Mauchamp & Atkinson, 2011) and the highlands are heavily invaded by blackberry (Rubus niveus), quinine (Cinchona pubescens), and invasive herbs (Jäger et al., 2009; Jäger et al., this volume). This is the only island where some long-term landbird monitoring has been carried out. A comparison of bird counts between 1997 and 2008 revealed that six of nine surveyed species had seriously declined (Dvorak et al., 2012; Figure 2). Of these, five are insectivorous species: large tree-finch,

green warbler-finch, woodpecker finch, yellow warbler, and vermilion flycatcher. Monitoring data (2008-2015) from the arid, agricultural, and fern zones showed that for some species and habitat types, the observed decline has not continued, with numbers seeming to stabilize around the lower values calculated in 2008. Counts from the remaining Scalesia habitat are highly variable. The green warbler-finch continues to decline in this fragile forest as in the fern zone, its two remaining strongholds. The small tree-finch, seemingly stable between 1997 and 2008, is now decreasing in the highlands. Large tree-finch numbers are low; this species needs special attention in the future. Galapagos doves, formerly common, are now rare especially around inhabited areas, but might have refuges in the northern arid zone where few counts have been conducted. Vermilion flycatchers are now so rare that they cannot be assessed with the point count method. According to specific searches done in 2015, the population estimate is around 30 to 40 breeding pairs with core zones north of El Puntudo and north of Los Gemelos around the red gravel mine. Ground finches are expanding further into the highlands, probably due to an increase in open habitat and many introduced small herb species now present in the Scalesia and fern zones, providing a seed source. Smooth-billed anis are encountered throughout the island, though numbers have declined since 2008, probably due to control measures by the GNPD.

Principal reasons for population declines and recommended priority actions Threat 1 – Philornis downsi

In the late 1990s, a highly invasive parasitic fly, P. downsi, was found to be significantly impacting reproductive output of most small landbirds (reviewed in Kleindorfer et al., 2014b). This fly is found throughout the Archipelago (Table 2) affecting many landbird species (Table 1). P. downsi is classified as one of the most invasive species in Galapagos (Causton et al., 2006) and is the most serious threat for many landbirds. Parasite-induced nestling mortality is high. Beak and naris deformation persisting into adulthood (Galligan & Kleindorfer, 2009) can affect courtship (birds sing differently) or make birds vulnerable during times of food scarcity.

Actions. Research on the biology and ecology of P. downsi must continue to find methods to reduce fly populations and protect landbirds. The international Philornis working group, comprising 20 institutions from eight countries, is evaluating potential short-term control methods, such as in situ nest treatment and fly trapping, until low-risk methods for permanent suppression of P. downsi over large areas are developed. Potential methods include biological control using natural enemies and the Sterile Insect Technique.

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Arid Transition Farmland Scalesia Fern

1997 - 2008

2008 -2014-15

1997 - 2008

2008 -2014-15

1997 - 2008

2008 -2014-15

1997 - 2008

2008 -2014-15

1997 - 2008

2008 -2014-15

Small ground-finch S S S S V V V V S I

Medium ground-finch I S S S S V IR V A I

Common cactus-finch S S A A A A A A A A

Vegetarian finch S S S S D S IR IR A A

Small tree-finch S S S S S D S V S S

Large tree-finch D D S S V V S V A A

Woodpecker finch D S S S D S D V S S

Green warbler-finch IR IR D S D S D D S D

Yellow warbler D S V D D S V V D I

Figura 2. Trends in the relative abundance of eight Darwin’s finches and the yellow warbler across five vegetation zones in Santa Cruz between 1997-2008 (adapted from Dvorak et al., 2012) (left column / habitat) and between 2008 and 2014/15 (right column / habitat).

Color and letter code: grey (A) = bird species not recorded; light yellow (IR) = irregular visitor; yellow (V) = fluctuations with no clear trend; green (I) = increasing; light green (I) = increased in comparison with 2008, but numbers have not reached values from 1997; blue (S) = number of birds is stable throughout the period 1997-2015; light red (S) = no further decline, numbers are around values from 2008; red (D) = numbers continue to decrease. Bold cells indicate stronghold habitat zones for each species.

Threat 2 – Introduced vertebrate species

In Galapagos, introduced rodents and cats (Felis silvestris) are known bird predators (Fessl et al., 2010a; Harper & Carrión, 2011; Konecny, 1987); while cats only occur on inhabited islands, black rats (Rattus rattus) and mice (Mus musculus) are widespread (Phillips et al., 2002). No significant rat predation on landbird nests was observed in the highland Scalesia forest (O’Connor et al., 2010b - Floreana; Cimadom et al., 2014 – Santa Cruz), but heavy predation by black rats has been observed in the lowlands of Floreana (O’Connor et al., 2010b) and on mangrove finch nests (Fessl et al., 2010b). Impacts of mice or the introduced smooth-billed ani — a potential predator, disease vector, and food competitor — are largely unknown.

Actions. Rat, cat, and smooth-billed ani monitoring and control are important for threatened native and endemic birds. On inhabited islands, increased efforts to decrease rat and cat populations are important in particular in agricultural areas, which are key habitats for some tree finch species. Expanding the cat sterilization program would help reduce cat populations. A better understanding of the ecology of the smooth-billed ani will help determine the need and feasibility of an eradication plan. Currently, Sophia Cooke (Cambridge University), with CDF and GNPD, is studying its ecology, and developing different trapping designs for a targeted removal of smooth-billed anis.

Threat 3 – Diseases and disease vectors

Diseases (e.g., avian pox) and animals that are potential disease vectors (e.g., the mosquito Culex quinquefasciatus, potential vector of avian malaria, and cats, vectors of Toxoplasma) are now present in

Galapagos with higher incidences on inhabited islands (Kilpatrick et al., 2006; Deem et al., 2011; Parker et al., 2011). Several strains of Plasmodium were identified in Galapagos (Levin et al., 2013). Pathogens can impact passerine survival and even lead to extinction (Van Riper et al., 1986; Dunn et al., 2013). The most important challenge for Galapagos is the prevention of future introductions.

Actions. Baseline health monitoring including monitoring of avian pox is well underway for many bird species (Parker & Deem, 2012). The collaborative project between University of Missouri, Wild Care Institute Saint Louis Zoo, GNPD, and CDF to collect baseline data on blood parasites needs to be continued and expanded. Protocols for avian disease prevention need to be developed and efforts to reduce mosquito vectors need to be supported as much as possible.

Threat 4 – Habitat degradation

Major habitat changes have occurred on inhabited islands because of human settlements and on uninhabited islands due to introduced herbivores. Almost all humid highland forests on inhabited islands were cleared for agriculture. The humid Scalesia forest, a prime habitat for tree finches, is a fraction of its original extension on Santa Cruz, Santiago, southern Isabela, and San Cristóbal. Herbicide use to control invasive plants may have secondary impacts on landbirds through reduced food availability (Jäger et al., this volume; Cimadom et al., 2014), while pesticides may also be affecting native birds (Hallmann et al., 2014).

Actions. The protection and restoration of the last remnants of Scalesia forest on Santa Cruz, San Cristóbal,

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and Floreana Islands have highest priority. The agricultural zones are refuges for several bird species, and efforts should focus on encouraging bird-friendly agricultural practices with minimal use of eco-friendly herbicides and insecticides, and habitat management, e.g., the replanting of native trees, especially Scalesia and Galapagos guava. Incentive schemes could be implemented such as the Bird Friendly Seal of Approval (Smithsonian Migratory Bird Center) or special recognition given to farms that protect nesting sites of native species.

An action plan and protection of the last refuges of the vermilion flycatcher on Santa Cruz are urgently needed and should include control of P. downsi, rodents, cats, and the invasive blackberry (without the use of herbicides). A management plan is also needed for El Cura on southern Isabela, where the vermilion flycatcher prefers old guava stands; guava removal from the park area would highly impact the population. A long-term plan for the replacement of guava by less invasive trees is needed. Lastly, an impact study of currently used pesticides on invertebrate communities and bird health is needed.

Threat 5 – Road kill

A census conducted by the GNPD on Santa Cruz in 2013 (Los Gemelos to Canal Itabaca) revealed that during three months (breeding season) more than 1000 birds were killed, 90% of which were yellow warblers. Short-eared owls (Asio flammeus) and barn owls (Tyto alba) have also been found killed regularly (A. Carrión, pers. com.). The impact of road kill on bird communities overall is unknown.

Actions. We need to investigate the impact of road kills on populations of the most affected species. More speed bumps or section control units are needed in critical areas, especially in the section through Los Gemelos to Canal Itabaca. In the long-term, a more ecological transport system, favoring buses to the canal, should be sought for Santa Cruz.

Conclusions

The threats to landbirds are not mutually exclusive; when

combined with natural population fluctuations caused by stressors such as climatic extremes they can seriously affect nesting success, survival (Cimadom et al., 2014; Koop et al., 2015), and recruitment. For example, habitat alteration can lead to reduction in food for birds that are then less able to compensate for the effects of parasitism by P. downsi. It is important to understand the impact of the different factors on birds and the interactions between them in order to develop and implement management actions to prevent further losses.

Data presented from Santa Cruz show the importance of long-term monitoring to detect bird population changes. The aim over the next few years is to establish an institutional long-term monitoring program for all islands >5 km2 in size, with special focus on islands with single island endemics or small, distinct populations. As all quantitative counting methods need specially trained personal, the involvement of Ecuadorian ornithologists in monitoring programs must be expanded.

Citizen science can and should help for easy-to-recognize species (Table 1). Together with the company “Birds in the Hands”, LLC, we have developed a free Galapagos Bird App that provides pictures and information to help in bird identification. This app will be promoted, and residents, tourists, naturalist guides, and park rangers invited to report bird sightings via eBird. A program has already been initiated with some tour operators to get site-specific data for birds with important knowledge gaps, such as the Galapagos martin. In conjunction with a professionally led monitoring program, we hope to collect usable data and, at the same time, raise awareness and increase local involvement.

Acknowledgments

The Galapagos Landbird Plan, implemented jointly by the Charles Darwin Foundation and the Galapagos National Park Directorate, is funded by Galapagos Conservancy and the International Community Foundation (with a grant awarded by The Leona M. and Harry B. Helmsley Charitable Trust). Fieldwork on Floreana was partially funded by Island Conservation. A special thank you to Andre Mauchamp for comments on a former draft and help in editing.

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Long-term conservation management to save the Critically Endangered mangrove finch (Camarhynchus heliobates)Francesca Cunninghame¹, Birgit Fessl¹, Christian Sevilla², Glyn Young³ and Nicole La Greco⁴

¹Charles Darwin Foundation²Galapagos National Park Directorate³Durrell Wildlife Conservation Trust⁴San Diego Zoo Global

Photo: © Francesca Cunninghame

Introdution

The Critically Endangered mangrove finch (Camarhynchus heliobates) (Birdlife International, 2016), is the rarest bird in the Galapagos Islands and in need of intensive conservation management to ensure its survival (Fessl et al., 2010a, 2010b; Cunninghame et al., 2015). With an estimated population of 100 individuals found in 30 ha of habitat on the remote northwest coast of Isabela Island, it is one of the most range-restricted birds globally (Fessl et al., 2010a, 2010b; Young et al., 2013). Although historically distributed throughout the mangrove forests of Isabela and Fernandina, an extensive reduction in range occurred from the early 1900s to the present (Dvorak et al., 2004). Causes of the decline, although not completely known, likely include predation from introduced species, and habitat change and loss (Fessl et al., 2010a, 2010b; Young et al., 2013). Currently the remaining mangrove finch population is threatened by nest predation from introduced black rats (Rattus rattus), nestling parasitism from the larvae of the introduced fly Philornis downsi, small population size, lack of genetic diversity, hybridization with the closely related woodpecker finch (C. pallidus), and potential habitat loss from volcanic activity and climate change (Fessl et al., 2010a, 2010b; Causton et al., 2013; Dvorak et al., 2004; Young et al., 2013; Cunninghame et al., 2015; Lawson et al., in prep).

Research on the remaining mangrove finch population and potential conservation management methods has been conducted since the 1990s. The Mangrove Finch Project, a bi-institutional initiative of the Charles Darwin Foundation (CDF) and the Galapagos National Park Directorate (GNPD) in collaboration with Durrell Wildlife Conservation Trust begun in 2006, has conducted in situ conservation management at Playa Tortuga Negra (PTN) and Caleta Black (CB) in an attempt to ensure the on-going survival of the species (Fessl et al., 2010b; Cunninghame et al., 2015). Management actions were developed based on research results, including the identification of nest predation from introduced rats as the main cause of nest failure (Fessl et al., 2010a, 2010b). The aim of the Mangrove Finch Project is to increase the population size and range of the species (Fessl et al., 2010b).

The Mangrove Finch Action Plan 2010-2015 (Fessl et al., 2010b), developed at a stakeholder workshop in 2009, has guided conservation management over the last five years. However, ongoing field research revealed extremely high nestling

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mortality due to P. downsi larvae parasitism, which had not been evident until rat control measures were in place (Cunninghame et al., 2015). This highlighted the importance of thorough field research and resulted in additional management methodologies.

A stakeholder workshop in 2015 assessed past and present conservation management of the species, resulting in the development of the 2016-2020 Mangrove Finch Conservation Action Plan. This plan incorporates all past research and management to ensure the most effective conservation management for the species over the next five years. Management of the species is both time intensive and expensive. Due to the precarious situation of the mangrove finch, it is vital to ensure that all techniques used result in the successful conservation of the species.

This article describes past and current management actions, provides an evaluation of results in relation to the long-term goals, and presents the next steps in the process.

Captive assurance population: 2007-2009

Due to the extremely small population size of the mangrove finch, the feasibility of a captive assurance population was assessed (Fessl et al., 2010b). A trial with the more common, closely related woodpecker finch was conducted using specially built infrastructure in Puerto Ayora (Fessl et al., 2010a; Good et al., 2009). Ten individuals were held for up to 18 months, and although all birds survived and were released into the wild following the trial, due to logistical complications and disease risk, the establishment of a captive mangrove finch population

was deemed unfeasible (Fessl et al., 2010b). Consequently, mangrove finch conservation management maintained an in situ focus with the aim of protecting and increasing the wild population (Fessl et al., 2010b).

Introduced rat control: 2007 to the present

Introduced rat control at PTN and CB was initiated in 2007, with the installation of over 200 enclosed bait stations containing wax cube Klerat baits (0.01 parts per million brodifacoum per kg). These are laid out in a 50-m grid throughout and around the periphery of the mangrove forests (Fessl et al., 2010b), and checked regularly and re-baited as necessary. Monitoring of introduced rats has revealed a reduction in rat numbers, while mangrove finch nesting success showed an increase from 18 to 37 percent (Fessl et al., 2010a). In recent years, mangrove finch nest predation by rats has been relatively low, representing just 13% of failed nests (Figure 1).

Due to continual reinvasion by rats into the mangroves, baiting must be constant to ensure that rat numbers are maintained at a low level and nest predation is low. Current rat control methods are successful in maintaining rats at a low density; however, the long-term regular use of brodifacoum is against best practice policy according to other countries due to the buildup of brodifacoum in the environment (Brown et al., 2015). Footprint tracking (ink tunnel monitoring) of bait station consumption in 2010-2011 revealed that even when rat numbers are low, invertebrates consume up to 30 g of bait per night per bait station. Consequently, the amount of bait deployed has been significantly reduced and rat monitoring intensified from twice to four times a year. The current action plan proposes an adoption of more reactive control methods

Failure: Nestling mortality

P. downsi

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Figure 1. Percentage of mangrove finch nests that fledged and causes of failure from 33 wild monitored nests over three seasons 2014-2016. Sample sizes differ between years (2014 n = 18, 2015 n = 11, 2016 n = 4), and were very low in 2016 due to an early and short breeding season caused by arid conditions. Nests are categorized as successful if at least one individual from a clutch fledges; no complete clutches have fledged with at least one nestling dying as a result of P. downsi parasitism in all monitored nests. The single fledgling observed in 2016 was treated in situ by the field team one day prior to it fledging when nine P. downsi larvae were removed from its nares and ears; its untreated clutch mate did not survive.

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to further reduce the amount of bait used, by monitoring with chew cards over larger areas and focusing control only in the areas where rats are detected. Moreover, self-resetting, multi-kill traps (Goodnature New Zealand) could be trialed on a small scale as a low maintenance non-toxic control method (Carter et al., 2016). Additionally, plans are underway to change to a less cumulative toxin, in conjunction with Island Conservation (IC) and the GNPD.

Translocation: 2010

Expanding the range of the mangrove finch to reduce the risk of extinction by establishing additional populations within the historic range on Isabela is a priority (Fessl et al., 2010b; Cunninghame et al., 2011), especially since the disappearance of the remnant population from southeastern Isabela in 2009 (Cunninghame et al., 2013). A trial translocation moving nine birds from PTN to Bahia Urbina was conducted in 2010 (Cunninghame et al., 2011; Cunninghame et al., 2013; Young et al., 2013). Long-term establishment did not occur and four of the nine individuals have since been observed at the source population (Cunninghame et al., 2013). Although the reestablishment of mangrove finches within their historic range continues to be a priority, the further translocation of juveniles or adults from PTN and/or CB has been suspended due to the lack of a sizeable source population from which to take individuals (Cunninghame et al., 2015). Any future attempts to establish individuals in other areas should be done using juveniles reared in captivity from eggs that have a lower probability of survival in the wild. Moreover, juveniles of certain species fledged at a new location are less likely to return to their natal site (Powesland et al., 2013).

Philornis downsi control: 2012 to the present

Field research from 2010–2014 highlighted the impact of P. downsi parasitism on mangrove finch nestling survival (Young et al., 2013; Cunninghame et al., 2015). Since 2011, this has been the principal cause for nest failure (Cunninghame et al., 2015) (Figure 1). In collaboration with the Philornis Project (CDF/DPNG), trapping trials have been conducted in mangrove finch habitat and the surrounding lava field since 2013 (Figure 2).

Trapping at PTN, although using the same lures deployed with relative success on Santa Cruz, has not shown any evidence of success even in localized protection for individual nests. There is still no viable method to protect mangrove finch nestlings in situ, which is a desired outcome for the conservation of the species (Causton et al., 2013). Current research into treating nests of other passerine species on Santa Cruz could potentially offer a viable method for protecting mangrove finch nestlings in situ.

Head-starting: 2014 to the present

In order to increase the number of fledglings produced each season, head-starting of early laid mangrove finch clutches has taken place for three consecutive years in collaboration with San Diego Zoo Global (SDZG) (Cunninghame et al., 2015). Artificial egg incubation and hand-rearing of nestlings in captivity, away from the presence of P. downsi parasitism, has enabled 36 mangrove finch fledglings to be released over the past three seasons (Figure 3).

Figure 2. Placement of McPhail traps for capture of adult Philornis downsi within and around the mangrove forest at PTN from 2012 to the present. Source: A Mauchamp

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2014 2015 2016 0

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Figure 3. Number of captive-reared fledglings released and successful wild fledglings from 33 monitored nests during three seasons 2014–2016 since head-starting was initiated. The single wild fledgling recorded for 2016 is certainly fewer than the actual number of fledglings due to only four nests being monitored. This occurred as a result of arid conditions causing a short mangrove finch breeding season, which ended while the field team was in Puerto Ayora for head-starting. From post-breeding field monitoring it is estimated that at least three wild fledglings were produced in 2016, although the nests which produced them were not monitored and their parentage unknown.

Figure 4. Captive-reared juvenile mangrove finches post release showing their unique color band combinations.

Life history traits of the species, especially their cryptic behavior when not breeding, make monitoring of non-breeding individuals unreliable (Fessl et al., 2011; Cunninghame et al., 2015). Moreover, initial dispersal

data suggest that young birds use habitat outside of the mangroves (Figures 5 & 6); whether juvenile birds spend long periods in the arid zone is unknown.

Overall head-starting has been a success, especially when compared to the relatively small number (fewer than 20) of wild fledglings produced (Figure 3). However, logistical challenges (delayed transport time of eggs from the field to captive-rearing facility) and complications with equipment and captive-husbandry in 2015 highlighted the importance of establishing best practice protocols for captive-rearing. Initial short-term telemetry monitoring

of released juveniles, following a soft release, has shown 97% survival during the 21-day period while transmitter batteries lasted. Nonetheless, the long-term impact of head-starting to increase population size remains unknown. After radio-tracking ends, captive-reared mangrove finches can only be identified by observing the unique color band combinations on their right leg (Figure 4).

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Figure 5. Dispersal of 36 captive-reared juvenile mangrove finches released from the aviary in the mangroves at PTN 5 to 24 days post release over three seasons of head starting. All individuals for each year are represented with the same color. Purple: 2014 n = 13; Blue: 2015 n = 8; Yellow: 2016 n = 15. Source: A Mauchamp

Figure 6. Dispersal of eight individual captive-reared juvenile mangrove finches (each individual represented by a different color) 3 to 24 days post release from the 2015 head starting season, PTN. Source: A Mauchamp

In order for head-starting to be a successful management technique, captive-reared birds must be recruited into the breeding population (Snyder et al., 1996). For the mangrove finch, recruitment of juvenile birds into the breeding population appears to take several years during which time it is difficult to obtain reliable data regarding the survival of captive-reared individuals. To date three captive-reared individuals (Figure 7) have been observed two and one year post release, one of which was calling with the correct mangrove finch call. These observations demonstrate that captive-reared mangrove finches are capable of longer-term survival in the wild. During the

next two years, any observations of juveniles released in 2014-2015 establishing territories or breeding will indicate success of head-starting juveniles.

Head-starting is planned for four consecutive seasons through 2017. A subsequent evaluation will determine its success as a tool for increasing the size of the mangrove finch population. Whenever a method for in situ protection of nestlings from P. downsi parasitism is deemed viable and the population appears to be in recovery, head-starting should be discontinued.

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Figure 7. One of three captive-reared mangrove finches from previous years that was observed at PTN in 2016, caught in a mist net during wild population capture and marking on 11 May 2016. It was weighed and released. This individual, hand reared and released in May 2015, was radio-tracked entirely in arid zone vegetation around Tagus Cove and the western base of Darwin Volcano for 12 days post release before its signal was lost. It was never located in the mangrove forest and it was unknown whether it would ever return to PTN.

Genetic diversity in the wild population

Collection of mangrove finch blood samples for genetic analysis has been conducted with the wild population since 1999; additionally, all captive-reared juveniles are sampled (Fessl et al., 2010b; Cunninghame et al., 2015; Lawson et al., in prep). Recent analysis (L. Lawson) shows a reduction in genetic diversity of the current population when compared to samples collected in 1899 and 1906, which represent the more widespread and populous historic population. Since captive-rearing was initiated in 2014, it has been possible to conduct paternity studies to better understand the breeding ecology of the mangrove finch. This has shown two incidences of extra pair copulations (where the female of a nesting pair copulates with another male but continues to nest with her original mate) (Lawson et al., in prep). The extent to which genetics can be used to help maximize conservation management of the mangrove finch is to be determined. Ideally, if head-starting is continued, to help reduce over-representation of certain individuals within the population, eggs should be collected from a diverse range of breeding pairs. However, with fewer than 20 breeding pairs remaining (Cunninghame et al., 2015), coupled with the even lower number of pairs with nests during the collection period, it is likely that in future years all available nests will be collected regardless of whether offspring from the same pair have been reared in the past.

To date, over the three seasons, mangrove finch fledglings from 16 different pairs have been released back into the wild. At least four of these pairs later reared their own offspring. An extra-pair copulation of an unbanded female woodpecker finch (who had paired with a known banded male mangrove finch) with a male woodpecker finch and

not recognised until later, resulted in two pure woodpecker finch eggs being collected for head-starting in 2014 and the juveniles released (Lawson et al., in prep) (Figure 8). This example highlights the importance of information gained from genetic sampling and analysis; however, few changes can be made to management techniques in the field if un-observed copulations sire offspring.

Recommendations for conservation management of the mangrove finch: 2016–2020

Conservation management of the mangrove finch is required in the near to mid-term to ensure that the population survives and expands (Fessl et al., 2010a; Fessl et al., 2010b; Cunninghame et al., 2015). Conservation of the species should be focused on the wild population, with any birds reared in captivity being released at the end of each breeding season as independent juveniles. A combination of complementary research and management is required in order to ensure that the actions succeed in reaching the long-term goal of increasing the population and range of the mangrove finch. The following management recommendations for the upcoming five years are proposed:

• Conduct seasonal monitoring of the mangrove finch population (point counts, territory mapping, and nesting-breeding success) to determine population dynamics, and identify any downward trends;

• Conduct in situ introduced rat control to ensure that nest predation is maintained at a low percentage; adopt best practice techniques;

• Collaborate with the Philornis Project, and conduct

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Figure 8. Four captive-reared fledglings from 2014: the two on the left are woodpecker finch (C. pallidus) siblings and the two on the right are mangrove finches (C. heliobates). Diagnostic plumage differences (yellower and clearer in C. pallidus, and darker and speckled in C. heliobates) are represented by individuals from both species.

field trials of new trapping techniques and individual nest treatment methods at PTN;

• Conduct head-starting for a minimum of one more season (totaling four), rearing at least eight individuals per season;

• Publish mangrove finch head-starting protocols during 2016;

• Continue to focus on building capacity within local partners and collaborators to lessen reliance on international assistance;

• Conduct monitoring of mangrove finch habitat to better determine long-term survival of captive-reared individuals;

• Use the thorough habitat assessment information (Dvorak et al., 2004) to select a potential reintroduction site for captive-reared individuals if no natural dispersal to other mangrove sites is confirmed prior to 2018-2019;

• Continue to collect genetic samples and work with collaborators for analysis to better inform management decisions;

• Repeat Population Viability Analysis taking into

account new parameters not included in the 2009 analysis, most notably the impact of P. downsi parasitism and head-starting;

• Maintain political and financial support to ensure that active conservation management of the Critically Endangered species continues.

Acknowledgements

The bi-institutional Mangrove Finch Project of the Charles Darwin Foundation and the Galapagos National Park Directorate in collaboration with San Diego Zoo Global and Durrell Wildlife Conservation Trust is currently funded by Galapagos Conservation Trust, Marguerite Griffith-Jones, GESS Charitable Trust, Decoroom Limited, The Leona M. and Harry B. Helmsley Charitable Trust, International Community Foundation, Swiss Friends of the Galapagos, Foundation Ensemble, the British Embassy in Quito, and several individual donors. The challenging field work would not have been possible without the continued outstanding commitment and motivation of local and international field assistants and volunteers.

ReferencesBirdLife International. 2016. Species factsheet: Camarhynchus heliobates. Downloaded from http://www.birdlife.org on 11/08/2016. Recommended citation for factsheets for more than one species: BirdLife International (2016) IUCN Red List for birds. Downloaded from http://www.birdlife.org on 11/08/2016.

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Brown K, G Elliott, J Innes & J Kemp. 2015. Ship rat, stoat and possum control on mainland New Zealand, an overview of techniques, successes and challenges. New Zealand Department of Conservation.

Carter A, S Barr, C Bond, G Paske, D Peters & R van Dam. 2016. Controlling sympatric pest mammal populations in New Zealand with self-resetting, toxicant free traps: a promising tool for invasive species management. Biological Invasions 18 (6): 1723-1736.

Causton CE, F Cunninghame & W Tapia. 2013. Management of the avian parasite Philornis downsi in the Galapagos Islands: a collaborative and strategic action plan. 167-173. In Galapagos Report 2011-2012. GNPS, GCREG, CDF and GC. Puerto Ayora, Galapagos, Ecuador.

Cunninghame F, HG Young & B Fessl. 2011. A trial conservation translocation of the mangrove finch in the Galapagos Islands, Ecuador. In Global Reintroduction Perspectives 3 (ed PS Soorae). Pp 151-156. IUCN/SSC, Abu Dhabi.

Cunninghame F, HG Young, C Sevilla, V Carrión & B Fessl. 2013. A trial translocation of the critically endangered mangrove finch: Conservation management to prevent the extinction of Darwin´s rarest finch. 174-179. In Galapagos Report 2011-2012. GNPS, GCREG, CDF and GC. Puerto Ayora, Galapagos, Ecuador.

Cunninghame, F., R. Switzer, B. Parkes. G. Young, A. Carrión, P. Medranda & C. Sevilla. 2015. Conserving the critically endangered mangrove finch: Head-starting to increase population size. 151-157. In Galapagos Report 2013-2014. GNPD, GCREG, CDF and GC. Puerto Ayora, Galapagos, Ecuador.

Dvorak M, H Vargas, B Fessl & S Tebbich. 2004. On the verge of extinction: a survey of the Mangrove Finch Cactospiza heliobates and its habitat on the Galapagos Islands. Oryx 38:1-9.

Fessl B, H Vargas, V Carrión, R Young, S Deem, J Rodríguez-Matamoros, R Atkinson, O Carvajal, F Cruz, S Tebbich & HG Young (Eds.). 2010a. Galapagos Mangrove Finch Camarhynchus heliobates Recovery plan 2010-2015. Durrell Wildlife Conservation Trust, Charles Darwin Foundation, Galapagos National Park Service.

Fessl B, HG Young, RP Young, J Rodríguez-Matamoros, M Dvorak, S Tebbich & JE Fa. 2010b. How to save the rarest Darwin’s finch from extinction: The Mangrove Finch on Isabela Island. Phil. Trans. Roy. Soc. Lond. Ser B 365:1019-1030.

Fessl B, AD Loaiza, S Tebbich & HG Young. 2011. Feeding and nesting requirements of the critically endangered Mangrove Finch Camarhynchus heliobates. J. Ornithology 52:453-460.

Good H, E Corry, B Fessl & S Deem. 2009. Husbandry guidelines for woodpecker finch (Camarhynchus pallidus) at Charles Darwin Foundation. 31 Pp. Internal Report CDF, Durrell Wildlife Conservation Trust.

Lawson LP, B Fessl, FH Vargas, HL Farrington, HF Cunninghame, JC Mueller, E Nemeth, PC Sevilla & K Petren. In preparation. Slow motion extinction: inbreeding, introgression, and loss in the critically endangered mangrove finch (Camarhynchus heliobates). Unpublished manuscript.

Powesland RG, M Bell, EA Tuanui, BM Tuanui & JM Monks. 2013. Translocation of juvenile Chatham Islands tomtits (Petroica macrocephala chathamensis) from Rangatira and Pitt Islands to Chatham Island. Notornis 60(1):41-48.

Snyder, NFR, SR Derrickson, SR Beissinger, JW Wiley, TB Smith, WD Toone & B Miller. 1996. Limitations of captive breeding in endangered species recovery. Conservation Biology 10(2):338-348.

Young HG, F Cunninghame, B Fessl & FH Vargas. 2013. Mangrove finch Camarhynchus heliobates an obligate mangrove specialist from the Galapagos Islands. In Mangrove Ecosystems (eds G Gleason & TR Victor). Pp 107-121. Nova Science Publishers Inc. New York.

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Natural history and conservation prospects of the Floreana mockingbird (Mimus trifasciatus)Luis Ortiz-Catedral1, Christian Sevilla2, Glyn Young3 and Danny Rueda2

1Massey University, New Zealand2Galapagos National Park Directorate3Durrell Wildlife Conservation Trust

Photo: © Luis Ortiz-Catedral

The Floreana mockingbird (Mimus trifasciatus) one of the bird species with the most restricted distributions in Galapagos and in the world, is found only on two islets: Champion and Gardner-by-Floreana, whose combined area is only 90 ha (Curry, 1986; Grant et al., 2000). Its current distribution is the result of its local extinction on Floreana Island where, according to subfossil records, it existed in the lowlands until the end of the 1800s (Steadman, 1986). Although the detailed chronology of this extinction of the Floreana mockingbird is not known, it is understood to be the result of the introduction of rodents and domestic cats, as well as habitat loss caused by fire and possibly other anthropogenic impacts (Curry, 1986). The combined effect of these factors is most likely responsible for the disappearance of six vertebrate species from Floreana Island from 1800 to the present (Estes et al., 2000; Grant et al., 2005; Steadman & Stafford, 1991).

The two remnant populations of the Floreana mockingbird represent a valuable demographic and genetic reservoir for the species, both for in situ conservation as well as an eventual reintroduction to its historic habitat on Floreana Island (CDF, 2008; Hoeck et al., 2010), following the planned eradication of introduced rodents and feral cats on the island (Island Conservation, 2013). In the short- and mid-term, it is important to determine the demographic trends of the Floreana mockingbird (Jimenez-Uzcategui et al., 2011), as well as obtain additional information about its biology, in order to develop a reintroduction strategy (CDF, 2008).

To date studies of the species have looked at genetic diversity (Hoeck et al., 2010), body condition and health (Deem et al., 2011), and diet during the breeding season (Ortiz-Catedral, 2014). However, two important aspects of the management of the species have not yet been documented: reproductive biology and the susceptibility of the chicks to parasitism by the phorid fly Philornis downsi. This article presents, for the first time, information on the nests and breeding season of Floreana mockingbirds, as well as observations on the presence of P. downsi. Finally we discuss population trends over the past five years and identify priorities for management of the species.

The information presented has been obtained thanks to the direct participation of numerous Galapagos National Park rangers, as well as volunteers and newly graduated Ecuadorian biologists. All participants received training in observation and mockingbird handling techniques, which represent a valuable addition to their abilities and experience in wildlife management. As a result, there is trained staff to meet the needs of conservation of this species in the short- and long-term.

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Methods

We visited the islets of Champion and Gardner-by-Floreana during the breeding season (between February and April) in 2011 and 2013, on trips with durations of four to seven consecutive days, to document the presence of active nests, the status of the nests, clutch size, the number of chicks per nest, and the composition of breeding groups. Once the chicks left the nest, we confirmed the cessation of reproductive activities, and recorded the physical characteristics of the nests and the presence or absence of P. downsi in the nest material. We also recorded the height of the nest and the plant species on which it was built. Approximately three weeks after hatching, the chicks were banded, using a unique combination of metal rings for each bird to allow individual identification. Each chick was inspected for damage in their nostrils caused by P. downsi (see Causton et al., 2013).

To estimate population size on both islets, we carried out surveys using the mark:recapture methodology described by Hoeck et al. (2010). The sampling area was equivalent to 20% of the total area of the current distribution of the Floreana mockingbird, and therefore the global population estimate is an extrapolation from the sampling area estimates.

Results

Nest characteristics

We recorded a total of 45 nests (five on Champion and 40 on Gardner-by-Floreana), at an average height of 1.2 ± 0.7 m (range 0.4 m to 4 m). The nests were built in four species of native plants: Croton scouleri (n=22), Cordia lutea (n=10), Gabrowskia boerhaaviaefolia (n=7), and Opuntia megasperma (n=6).

The nest is typically in the form of a cup. Viewing it from the top, the axes (n=5) measured 23.1 x 23.0 cm, with an average depth of 13.8 cm (± 1.7 cm). Each nest (n=8) consisted of approximately 198 ± 56 twigs that are 3-29 cm long, mainly of Gabrowskia boerhaaviaefolia, Croton scouleri, and Cordia lutea. Other nest-building materials included radius and ulna bones of frigatebirds (Fregata major), Nazca booby (Sula grantii) feathers, skin of the Galapagos snake (Pseudalsophis biserialis), and gecko (Phyllodactylus baurii) skin, as well as leaves of Scalesia affinis. Clutch size ranged from one to four eggs (average 2.5 eggs), with egg dimensions of 26.0 x 18.4 mm (n=2). Eggs were pale blue in color, with irregular brown spots (Figure 1).

Nest success and parasitism by Philornis downsi

Incubation lasts 15 to 17 days and chicks leave the nest 13 to 16 days after hatching. They tend to remain in the low vegetation a few centimeters from the base of the plant where the nest is located. Of the 45 registered nests, the emergence and development of chicks was only observed for 17 nests, which produced an average of 2.4 chicks (range 1-4 chicks). The rest of the observed nests failed due to egg predation (n=8), chick predation (n=5), abandonment (n=3), or unknown causes (n=12). Pupae of P. downsi were found in only five nests (11%) and never more than 25 pupae were detected. A total of 101 chicks and juveniles were banded; none of them had deformations in the nostrils or beak attributable to parasitism by P. downsi.

Deformations due to P. downsi were not observed in the 170 adult birds banded during the same period. Although circumstantial, these observations and the low incidence of nests with pupae of P. downsi indicate that this parasite occurs at lower levels in this species than in other species of Galapagos birds, including the Galapagos mockingbird

Figure 1. Nest and eggs of a Floreana mockingbird. Photo: L. Ortiz-Catedral ©

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(Mimus parvulus) (Knutie et al., 2016; O’Connor et al., 2010). It is not known which species prey on Floreana mockingbird eggs and chicks on Champion and Gardner-by-Floreana, but we have observed Floreana mockingbirds attacking groups of anis (Crotophaga ani) next to active nests. This species feeds on chicks of other birds (Connett et al., 2013). We have also seen Floreana mockingbirds attacking Galapagos snakes (Pseudalsophis biserialis), a species that we have observed inspecting active finch nests on Champion and Galapagos mockingbird nests on Santa Cruz Island.

Population estimate

The estimate of the global population of Floreana mockingbirds has ranged from a maximum of 696 individuals in November 2010, to a minimum of 435 individuals in June 2011. On average, the annual population size (2010-2012) is estimated at 578 individuals for the two islands (Figure 2). This population size is greater than that estimated between 2003 and 2007 (i.e., 85-231 individuals), using transect counts (Jimenez-Uzcategui et al., 2011).

Conclusions and recommendations

Floreana mockingbirds, unlike several finch species and Galapagos mockingbirds, appear to be less affected by P. downsi, as indicated by the low frequency of this parasite in the nests observed during this study, and the non-existent evidence of deformation of nostrils in juveniles and adults. Our observations are consistent with the theory of that the acute intensity of parasitism of P. downsi is associated with higher, humid areas in Galapagos (Wiedenfeld et al., 2007).

In planning a future reintroduction of the Floreana mockingbird to the island that it is named for, it would be important to ascertain that the potential release sites exhibit low levels of parasitism of P. downsi. This can be verified by means of a study of finch species that inhabit the lowlands of the island, as a precautionary measure to minimize any impact of this parasite in the future development of mockingbird chicks.

In general terms, the nesting of the Floreana mockingbird is similar to that of other mockingbird species in Galapagos. As suggested by Curry (1986), Floreana mockingbirds are not dependent on Opuntia megasperma for building nests. Therefore, the absence of Opuntia

megasperma in the lowlands of Floreana does not pose a limiting factor for the reintroduction of mockingbirds, because other species such as Croton scouleri, Cordia lutea, and Gabrowskia boerhaaviaefolia are common. Finally, our population estimates suggest that the inter-annual variability in population size is less drastic than previously estimated (see Jimenez-Uzcategui et al., 2011).

In general terms, the next steps for the conservation of the species include:

1. Development of an updated reintroduction plan with specific objectives and a general schedule of actions and their evaluation.

2. Development of a socialization plan with the community of Puerto Velasco Ibarra to identify local attitudes towards the reintroduction of an endemic species.

3. Identification of potential reintroduction sites in the

lowlands of Floreana, taking into account availability of food resources, structure of the habitat, and relative abundance of P. downsi.

4. Continuation of annual counts of the populations of

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Figure 2. Global population estimate for the Floreana mockingbird, based on censuses on Champion and Gardner-by-Floreana islets.

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Champion and Gardner-by-Floreana Islets to better understand the population dynamics of this species.

5. Continuation of training staff, volunteers, and Ecuadorian biologists.

Acknowledgments

We would like to thank Estalin Jiménez, José Naula, Alizón Llerena, Milton Chugcho, Johannes Ramirez,

Walter Chimborazo, Christian Pilamunga, Alonso Carrión, Fidelino Gaona, and to all the volunteers who helped in the field. We also thank Massey University, Durrell Wildlife Conservation Trust, Friends of Galapagos New Zealand, Mohamed bin Zayed Species Conservation Fund, Galapagos Conservation Trust, and Galapagos Conservancy Canada for financial support. The Charles Darwin Foundation provided valuable logistical assistance and the University of Zurich provided field teams to complete multiple trips to the study sites.

ReferencesCauston C, F Cunninghame & W Tapia. 2013. Manejo del parásito aviar Philornis downsi en las islas Galapagos: un plan de accion colaborativo y estratégico. Informe Galapagos, 2011-2012, 167-173.

CDF (Charles Darwin Foundation). 2008. The reintroduction of the Floreana mockingbird to its island of origin. Informe interno Fundacion Charles Darwin, Puerto Ayora, Galapagos.

Connett L, A Guezou, HW Herrera, V Carrión, PG Parker & SL Deem. 2013. Gizzard contents of the Smooth-billed ani Crotophaga ani in Santa Cruz, Galapagos Islands, Ecuador. Galapagos Research 68:7.

Curry RL. 1986. Whatever happened to the Floreana mockingbird? Noticias de Galapagos 43:13-15.

Deem SL, PG Parker, MB Cruz, J Merkel & PEA Hoeck. 2011. Comparison of blood values and health status of the Floreana mockingbirds (Mimus trifasciatus) on the islands of Champion and Gardner-by-Floreana, Galapagos Islands. Journal of Wildlife Diseases 47:94-106.

Estes G, KT Grant, & PR Grant. 2000. Darwin in Galapagos: his footsteps through the archipelago. Notes and Records, The Royal Society Journal of the History of Science 54:343-368.

Grant PR, RL Curry & BR Grant. 2000. A remnant population of the Floreana mockingbird on Champion Island, Galapagos. Biological Conservation 92:285-290.

Grant PR, BR Grant, K Petren & LF Keller. 2005. Extinciton behind our backs: the possible fate of one of Darwin’s finch species on Isla Floreana, Galapagos. Biological Conservation 122:499-503.

Hoeck PEA, MA Beaumont, KE James, BR Grant, PR Grant & LF Keller. 2010. Saving Darwin’s muse: evolutionary genetics for the recovery of the Floreana mockingbird. Biology Letters 6:212-215.

Island Conservation. 2013. Floreana Island Ecological Restoration: rodent and cat eradication feasibility analysis version 6.0. Internal Report Island Conservation, Santa Cruz, California.

Jiménez-Uzcátegui G, W Llerena, B Milstead, EE Lomas & DA Wiedelnfeld. 2011. Is the population of the Floreana mockingbird Mimus trifasciatus declining? Cotinga 33:1-7.

Knutie SA, JP Owen, SM McNew, AW Bartlow, E Arriero, JM Herman, E DiBlassi, M Thompson, JA Koop & DH Clayton. 2016. Galapagos mockingbirds tolerate introduced parasites that affect Darwin’s finches. Ecology 97:940-950.

O’Connor JA, FJ Sulloway, J Robertson & S Kleindorfer. 2010. Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Bioviersity and Conservation 19:853-866.

Ortiz-Catedral L. 2014. Breeding season diet of the Floreana mockingbird (Mimus trifasciatus), a micro-endemic species from the Galapagos Islands, Ecuador. Notornis 61:196-199.

Steadman DW. 1986. Holocene vertebrate fossils from Isla Floreana, Galapagos. Smithsonian Contributions to Zoology 413:103.

Steadman DW & T Stafford. 1991. Chronology of Holocene vertebrate extinction in the Galapagos Islands. Quaternary Research 36:126-133.

Wiedenfeld DA, G Jiménez-Uzcátegui, B Fessl, S Kleindorfer & JC Valarezo. 2007. Distribution of the introduced parasitic fly Philornis downsi (Diptera, Muscidae) in the Galapagos Islands. Pacific Conservation Biology 13:14-19.

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Giant Tortoise Restoration Initiative: Beyond rescue to full recovery Washington Tapia1, James P. Gibbs2, Danny Rueda3, Jorge Carrión3, Fredy Villalba3, Jeffreys Málaga3, Galo Quezada3, Daniel Lara3, Adalgisa Caccone4 and Linda J. Cayot1

1Galapagos Conservancy2State University of New York – College of Environmental Science and Forestry 3Galapagos National Park Directorate4Yale University – Department of Ecology and Evolutionary Biology

Photo: © James Gibbs

In the Galapagos Islands, giant tortoises have played an essential role as ecosystem engineers for over one million years, profoundly shaping the terrestrial landscape. As many as 200,000 giant tortoises once roamed the islands; today we estimate only some 10% remain (Figure 1). The tortoises’ dramatic decline was mainly due to overexploitation by whalers in the 1800s. Colonists killed tortoises as well until the 1950s, and introduced species, such as rats, pigs, and goats, preyed on tortoises and destroyed their habitat. Despite their reduced numbers, today giant tortoises play an important economic role as the Galapagos Islands’ single greatest eco-tourism attraction.

Much has been done to rescue giant tortoises from oblivion, the fate widely predicted for these creatures up to the 1940s, and a major motivation for scientific expeditions in the early 1900s to collect the last specimens while some still remained. The first major milestone was the establishment of the the Galapagos National Park in 1959. An initial focus was on determining the status of the giant tortoise populations. In 1965, the Charles Darwin Research Station (CDRS) initiated the giant tortoise breeding and repatriation program, which has become a world-class program, now run by the Galapagos National Park Directorate (GNPD). Since the first release of juvenile tortoises on Pinzón in 1970, more than 5,000 young tortoises have been repatriated to their island of origin. The recovery of the Española tortoise species (Chelonoidis hoodensis) from near extinction through a captive breeding program was another major milestone. This was followed in 2006 by the completion of Project Isabela, the largest ecosystem restoration initiative ever carried out in a protected area, which eliminated introduced goats—one of the biggest threats to giant tortoises—from northern Isabela, Santiago, and Pinta Islands (Carrión et al., 2011). Based on lessons learned and new developments in rodent eradication technology, the GNPD and its collaborators then completed the eradication of introduced rats on Pinzón Island in 2012; this has enabled hatchling tortoises to survive in situ for the first time in over 100 years (Tapia et al., 2015b).

Here we describe the chief components of the newly established Giant Tortoise Restoration Initiative (GTRI), which builds on the past 50 years of tortoise conservation efforts, to restore tortoise populations to their historical numbers throughout the Archipelago.

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A new era for giant tortoise restoration

In July 2012, an international workshop, Giant Tortoise Recovery through Integrated Research and Management, was held in Galapagos. Building on the accomplishments of the last half-century of tortoise conservation, the workshop generated strategic and operational plans to guide the next few decades of tortoise research and management.

These plans coalesced into the GTRI, initiated in 2014, as a collaborative effort of Galapagos Conservancy (GC), the GNPD, and a group of international scientists. The GTRI’s primary goal is to re-align and expand conservation efforts toward fully restoring the tortoise complex in numbers, range, ecological impact, and economic importance throughout the Archipelago.

To advance the GTRI, the GNPD provides technical and field expertise, logistical support, field personnel, infrastructure, and the authorization to carry out the work. GC provides overall coordination and leadership, scientific advice, and strategic funding; ultimately GC plans to invest more than $1,000,000 in tortoise restoration. The small team that oversees the GTRI and coordinates its suite of ambitious activities includes the Galapagos-based director of the Initiative (Tapia); the California, USA-based coordinator (Cayot); the New York, USA-based science advisor (Gibbs); and Galapagos National Park technicians

(Rueda and Carrión). Dr. Gisella Caccone leads the tortoise genetics team from her base at Yale University and provides critical guidance. The GTRI expands on decades of tortoise research and management investments, and is currently focused on the following priority projects. GTRI priorities for the next five years

Periodic review of the giant tortoise breeding and rearing centers. In November 2014, the first comprehensive review of the three Galapagos National Park tortoise breeding and rearing centers was carried out by a team that included tortoise experts, a veterinarian with expertise in Galapagos tortoises, and Galapagos National Park personnel. The team carried out visits to each center to review tortoise health, condition of tortoise corrals, infrastructure and equipment, maintenance, and personnel. The goal of the periodic review is to ensure that improved and consistent protocols are used at all centers. Salary support for a critical staff position has also been provided. Out-of-country professional “re-tooling” opportunities overseas are being funded and planned for selected center staff. Current plans are underway to renovate the technology for incubating tortoise eggs. Genetic analyses are currently being used to improve breeding programs, beginning with tortoises from Española and Pinzón.

Given that tortoise health issues, particularly of tortoises maintained in captivity, are of increasing concern, we have

Figure 1. Tortoise distribution in the Galapagos Islands (modified from Caccone et al., 2002).

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begun to compile and analyze the available information to identify problems and highlight knowledge gaps. In collaboration with personnel of the University of Armed Forces of Ecuador (ESPE – Spanish acronym), we are carrying out laboratory tests to develop protocols for parasite and disease detection in tortoise blood and scats. Return of giant tortoises to Santa Fe Island. Tortoises once lived on Santa Fe Island in the central part of the Archipelago but, sadly, the species has been extinct for more than 150 years. To address the situation, the GTRI conducted a careful review including the definitiveness of evidence of the former existence of an endemic Santa Fe tortoise, potential positive and negative impacts of tortoise restoration to the island’s ecosystem, possible sources of “analog” tortoises to replace the long-lost endemic form, and an evaluation of restoration alternatives based in part on modeling future tortoise reintroduction scenarios (Tapia et al., 2015a). On the basis of accumulated scientific knowledge, the GNPD implemented a plan to restore tortoises to the island using the genetically and morphologically similar Española tortoise (Poulakakis et al., 2011). In June 2015, 201 juvenile Española tortoises were released in the interior of Santa Fe Island (Figure 2). Annual releases of 60-80 tortoises are planned over the next ten years. Monitoring of tortoises, endemic land iguanas, and vegetation is carried out regularly. A 2016 resurvey confirmed that apparently all tortoises released had survived their first year, far exceeding the 50% survival rate expected. The island is relatively pristine and monitoring data will provide vital information about

how tortoises repopulate an island and their future effects on the ecosystem. Notably, Santa Fe also now holds an insurance colony of Española tortoises, listed as critically endangered by the IUCN.

Reestablishing giant tortoise populations on Pinta and Floreana Islands. One of the long-term goals of the GTRI is the reestablishment of reproductive tortoise populations on Floreana and Pinta Islands, where tortoises are now extinct. In addition to reestablishing historical tortoise populations, doing so will contribute to restoration of the islands’ ecosystems. Repopulation of these islands is being accomplished by recovering tortoises with significant levels of their genomes showing ancestry from either Floreana or Pinta from Wolf Volcano on Isabela Island. Wolf Volcano hosts an eclectic set of tortoises: a major GNPD-organized expedition in 2008 and subsequent genetic analysis of the blood samples collected (Garrick et al., 2012; Edwards et al., 2013) confirmed that tortoises were likely translocated to Wolf Volcano from around the Archipelago during the whaling era when large numbers of tortoises were not only killed but also moved around the islands. A major expedition, involving a large group of park rangers and collaborating scientists, a support helicopter, and a research vessel onsite throughout the expedition, was carried out in November 2015 (Figures 3-5). Thirty-two tortoises with shell features similar to the known Floreana and/or Pinta hybrids were transferred to the Fausto Llerena Tortoise Center on Santa Cruz Island and blood samples were taken from over 180 other tortoises with similar features that remain on the volcano. Detailed plans

Figure 2. Park rangers releasing juvenile giant tortoises from the Española Island lineage to Santa Fe Island in June 2015. Photo: GNPD

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for breeding programs are being developed to produce young tortoises to repopulate Floreana and Pinta Islands. Some tortoises, properly quarantined, may be transferred directly from Wolf Volcano to Floreana or Pinta. Tortoises in this program are expected to thrive when released on their home islands, as did the sterilized tortoises released

on Pinta Island in 2010 after a lifetime in captivity, gaining an average of 10 kg in the first year (Hunter, 2013). As on Santa Fe, monitoring programs will track the tortoises through the years following release on their new home islands.

Figure 3. Participants on the Wolf Expedition in November 2015 aboard the GNPD research vessel—Sierra Negra. Photo: Jane Braxton Little

Figure 4. The GNPD research vessel—Sierra Negra— with helicopter, at the base of Wolf Volcano, November 2015. Photo: Jane Braxton Little

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Defining the role of tortoises as keystone species and ecological engineers, and improving tortoise habitat. Re-conceptualizing giant tortoises not just as fascinating biological creatures but as agents of ecosystem dynamics, that is, as ecosystem engineers (Gibbs et al., 2009), has expanded the rationale for tortoise restoration. Tortoise restoration is not just about tortoises; it’s also about ecosystem restoration and, more generally, advancing island restoration in Galapagos. However, we do not yet fully understand how tortoises shape the ecosystems and biological communities in which they live. To this end, an elaborate system of tortoise “exclosures” centered around cactus, along with companion “control” plots, has been established on both Española and Santa Fe Islands (Figure 6). Annual monitoring is beginning to reveal the impact of tortoises on plant communities, especially cactus, in ways both positive (facilitating sexual reproduction via seed dispersal) and negative (eating pads and reducing asexual reproduction). A large-scale, archipelago-wide status survey of Opuntia, with emphasis on the lower, arid islands, is anticipated in the years ahead to better understand the status of these plants vital to the expansion of tortoise populations throughout the Archipelago.

Population surveys and advanced genetic sampling in San Cristóbal, Pinzón, southern Isabela, Santiago, and other islands. During the tortoise workshop in 2012, several knowledge gaps were identified, including the general lack of knowledge of the status of some extant populations, such as the Cerro Fatal tortoises, those of Wolf and Darwin Volcanos, and the San Cristóbal population. These will be the focus of intensive population surveys in the next few years. We also need additional knowledge of the genetic relationships and evolutionary distinctiveness of tortoises from different areas. In some cases, tortoise populations now considered one species should probably be classified as two or more distinct species. An example of a recently identified species, based on results of genetic analysis, is the eastern Santa Cruz Island tortoise (Chelinoidis donfaustoi) from the Cerro Fatal area, named in honor of the distinguished park ranger and tortoise caretaker Don Fausto Llerena (Poulakakis et al. 2015; Figure 7). GTRI seeks to facilitate collaborations between outside scientists and GNPD to combine modern genetic analysis with boots-on-the-ground surveys to help resolve the many unknowns about various tortoise populations, thereby fostering more effective conservation.

Fernandina exploration. Since 1906, with the collection of a single specimen on Fernandina by the California Academy of Sciences, there has been evidence that a mysterious species of giant tortoise—Chelonoidis phantastica—or fantastic giant tortoise might exist somewhere on the island. Since the specimen collected in 1906, there have been three independent observations (primarily tortoise scat) suggesting that a few tortoises may still remain on the largely unexplored island. There

has, however, never been an expedition to systematically search for the tortoises of Fernandina. The GTRI is working to catalyze a search across the island, using a combination of newly available high resolution satellite imagery, low‐level helicopter surveying, ground‐level exploration of the most promising tortoise hotspots identified from the air, and exploration of caves likely to contain remains of tortoises.

Genetic data are similarly puzzling. Mitochondrial DNA data suggest that the one individual collected shares a similar haplotype with tortoises from C. porteri from Santa Cruz, a haplotype that has never been found in the geographically closer southern and central Isabela species. This could suggest a recent human-mediated movement. However, given that the same haplotype has not been recovered in the extant population of C. porteri and that C. porteri is not saddleback as is the Fernandina specimen, it could be that Fernandina was colonized long ago by an ancestor of the same lineage that gave rise to C. porteri. In this second scenario, either through vicariance or dispersal through the Perry Isthmus, a few domed tortoises arrived on Fernandina and evolved into a new saddleback species. Ongoing genome-wide analyses will permit a test of these two hypotheses. Evaluation and mitigation of human interactions with and impact on giant tortoises. Giant tortoises were a traditional part of the diet of settlers in Galapagos. When the Galapagos National Park was established in 1959, efforts to curb the hunting of tortoises were generally successful. However, killing tortoises underwent a resurgence on Isabela Island in the 1990s (Cayot & Lewis, 1994) and has become a serious concern on southern Isabela, where the largest tortoise populations in the entire Archipelago once occurred, particularly on Sierra Negra. There, the human-tortoise conflicts need to be resolved. On Santa Cruz and San Cristóbal Islands there are increased road systems and infrastructure in the highlands that could be altering tortoise movements. An expanded program involving GTRI, along with the Galapagos Biosecurity Agency and the Charles Darwin Foundation, will generate guidelines to mitigate any identified problems; actions will potentially include education, community outreach, establishing migration corridors, adapting best management practices for habitat, and enforcement.

Lonesome George. Coincidentally the death of Lonesome George occurred on the eve of the convening of the international giant tortoise workshop in 2012. Amongst the tears and choked voices of workshop participants emerged a strong sentiment to realize the words inscribed on the information panel adjacent to Lonesome George’s old enclosure at the Fausto Llerena Tortoise Center: “Whatever happens to this single animal, let him always remind us that the fate of all living things on Earth is in human hands.” Lonesome George’s death inspired the workshop participants to “think big” and expand the

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Figura 6. Exclosures established on Santa Fe Island in 2014 (left; back one keeps tortoises out while the white one in front keeps both tortoises and land iguanas out); exclosure on Española (right). Photos: Washington Tapia (left), James Gibbs (right).

gains in tortoise conservation over the last 50 years. In very pragmatic terms, the GTRI has invested tremendous resources in preserving the conservation legacy of Lonesome George for the people of Ecuador and the larger world by orchestrating his temporary re-location to the New York City area to be taxidermied by world-class experts for return to Galapagos where the tortoise will be ensconced in the newly renovated tortoise rearing center visitation site (Figure 8). There he will continue to remind us of the constant need to work together to prevent future extinctions of all species. A beloved family member will also be able to rest back home again.

Prior to the workshop in 2012, an effort to sequence the entire genome of Lonesome George had begun. This collaborative effort is ongoing and involves an

international team including: the laboratories of Kevin White at the University of Chicago (USA), Carlos Lopez-Otin at the University of Oviedo (Spain), and the Caccone team at Yale. This work is paralleled by development of genome-wide markers (SNPs, Single Copy Polymorphic markers) to study the neutral and adaptive component of the Galapagos tortoise genome. This will provide insights on morphological and life history traits that make these animals unique, facilitate the identification of individuals of high conservation value for restoring threatened or extinct tortoise populations, and help to understand the relative importance of environmental features in shaping the existing genetic variability, which in turn will help to understand potential impacts of climate change on these animals.

Figure 5. Tortoises collected on Wolf Volcano arriving in Puerto Ayora (left) and settling into their new corral (right). Photos: Joe Flanagan

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Figure 7. Fausto Llerena and Eastern Santa Cruz Tortoise (Chelinoidis donfaustoi). Photo: Washington Tapia

Figure 8. The taxidermied Lonesome George on display at the American Museum of Natural History in September 2014. Photo: JargaPix Photography

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ReferencesCaccone A, G Gentile, JP Gibbs, T Fritts, HL Snell, J Betts & JR Powell. 2002. Phylogeography and history of giant Galápagos tortoises. Evolution 56(10):2052-2066.

Carrión V, CJ Donlan, KJ Campbell, C Lavoie & F Cruz. 2011. Archipelago-wide island restoration in the Galápagos Islands: Reducing costs of invasive mammal eradication programs and reinvasion risk. PLoS ONE 6(5):e18835. doi:10.1371/journal.pone.0018835

Cayot LJ & E Lewis. 1994. Recent increase in killing of giant tortoises on Isabela Island. Noticias de Galapagos 54:2-7.

Edwards DL, E Benavides, RC Garrick, JP Gibbs, MA Russello, KB Dion, C Hysenic, JP Flanagan, W Tapia & G Caccone. 2013. The genetic legacy of Lonesome George survives: Giant tortoises with Pinta Island ancestry identified in Galápagos. Biological Conservation 157:225-228.

Garrick RC, E Benavides, MA Russello, JP Gibbs, N Poulakakis, KB Dion, C Hyseni, B Kajdacsi, L Márquez, S Bahan, C Liofi, W Tapia & G Caccone. 2012. Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species. Current Biology 22(1):10-11.

Gibbs JP, EJ Sterling & FJ Zabala. 2009. Giant tortoises as ecological engineers: A long-term quasi-experiment in the Galápagos Islands. Biotropica 42(2): 208-214.

Gibbs JP, EA Hunter, KT Shoemaker, WH Tapia & LJ Cayot. 2014. Demographic outcomes and ecosystem implications of giant tortoise reintroduction to Española Island, Galapagos. PLoS ONE 9(10): e110742. doi:10.1371/journal.pone.0110742

Hunter EA, JP Gibbs, LJ Cayot & W Tapia. 2013. Equivalency of Galápagos giant tortoises used as ecological replacement species to restore ecosystem functions. Conservation Biology 27(4):701-709.

Poulakakis N, MA Russello, D Geist & A Caccone. 2011. Unraveling the peculiarities of island life: Vicariance, dispersal and the diversification of the extinct and extant giant Galápagos tortoises. Molecular Ecology 21:160–173.

Poulakakis N, DL Edwards, Y Chiari, RC Garrick, MA Russello, E Benvides, GJ Watkins-Colwell, S Glaberman, W Tapia, JP Gibbs, LJ Cayot & A Caccone. 2015. Description of a new Galapagos giant tortoise species (Chelonoidis; Testudines; Testudinidae) from Cerro Fatal on Santa Cruz Island. PLoS ONE 10(10): e0138779. Doi:10. 1371/journal.pone.0138779

Tapia W, D Rueda, L Cayot & J Gibbs. 2015a. Plan para la reintroducción de las tortugas gigantes a la isla Santa Fe como estrategia para su restauración ecológica. Technical report. GNPD.

Tapia W, J Málaga & JP Gibbs. 2015b. Giant tortoises hatch on Galapagos island. Nature 517:271.

Conclusion and next steps

The GTRI takes as its role model the first tortoises released to Española in 1971 by the GNPD and the CDRS; those tortoises initiated the recovery of a species that at one time was on the verge of extinction but now has a burgeoning population of more than 1000 tortoises thriving and reproducing on the island (Gibbs et al., 2014). In a similar slow, tortoise-like fashion, we hope that the programs we are launching during these first five years of the GTRI will provide the necessary seeds for an extended program of self-restoration and population growth by the tortoises themselves throughout the Archipelago. We are off to a good start thanks to the ideas generated at the 2012 tortoise workshop, the hard work and dedication of the GNPD, the collaboration of international scientists, and the spark that Lonesome George’s death produced to motivate us to strive even harder to restore the giant tortoise populations of Galapagos.

Please follow the GTRI blog at Galapagos Conservancy’s website for the latest news about this evolving, collaborative effort to fully restore these magnificent creatures.

Acknowledgments

We would like to thank all of those who have worked for tortoise conservation over the last half century, all of those who participated in the tortoise workshop in 2012, and all of the park rangers, volunteers, and scientists who continue to work with us to ensure that the GTRI is a success. We would also like to thank Galapagos Conservancy members who support these efforts, as well as the Phillips Family Foundation, Mohamed bin Zayed Species Conservation Fund, Fondation Ensemble, Lawrence Foundation, Oak Foundation, Turtle Conservancy, and other groups that provide support for the international scientists who are an integral part of the GTRI.

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Total number and current status of species introduced and intercepted in the Galapagos IslandsCharlotte E. Causton1, Heinke Jäger1, María Verónica Toral Granda2, Marilyn Cruz3, Manuel Mejía3, Erika Guerrero3 and Christian Sevilla4

1Charles Darwin Foundation2Charles Darwin University, Darwin, Australia3Galapagos Biosecurity Agency (ABG)4Galapagos National Park Directorate

Photo: © Heinke Jäger

Background

The number of species introduced to Galapagos has not been updated since 2008 (Atkinson et al., 2011). As a result of taxonomic revisions of some groups, there have also been changes in the status (e.g., naturalized, eradicated, etc.) of some species. Although this information can be found in the Datazone of the Charles Darwin Foundation (CDF), the current format of this database does not enable users to easily access updated information. Recognizing this, CDF is currently undertaking a new design for Datazone that will allow regular updates that include newly entered information.

Meanwhile, and as part of an assessment of the pathways of species that have been introduced to Galapagos, a comprehensive review was carried out of all databases that include information on introduced species. One of the objectives of this study was to determine their total number, how they arrived, and their status in Galapagos. It is important to emphasize that the Datazone database is dynamic and allows the entry of new records from local institutions, and data from scientific studies and surveys. The total numbers presented in this article represent the best information available at this date.

The classification of the pathways of species introduced to Galapagos follows the protocol designed by Hulme et al. (2008) and subsequently adopted by the Convention on Biological Diversity to address the problem of introduced species under Target 91 of the Aichi Targets of the Strategic Plan 2011-2020 of the United Nations Convention on Biological Diversity (CBD, 2014). Minor modifications were made to this protocol to better fit the reality of Galapagos.

Species that have been introduced and intercepted in Galapagos

To date, a total of 1579 species have been recorded as having been introduced or intercepted in Galapagos. This includes 821 (52%) terrestrial plants (including varieties and cultivars), 545 insects (34.5%), 77 other terrestrial invertebrates (4.9%), 63 pathogens (4%), 50 vertebrates (3.2%), 21 marine invertebrates (1.3%) and two marine plants (Table 1).

1 Aichi Target 9: By 2020, invasive alien species and pathways are identified and prioritized, priority species are controlled or eradicated, and measures are in place to manage pathways to prevent their introduction and establishment.

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Of this total, 82 species (mostly insects) were intercepted in transport vehicles or cargo during biosecurity inspections. These species are not established in Galapagos. Monitoring of transport vehicles allows the timely detection of alien species entering Galapagos and reduces the risk of establishment.

There are 17 species that are from historical records only (species may not have established or reports were erroneous). Four species have been eradicated under management programs: rock pigeon (Columba livia); tilapia (Oreochromis niloticus); kudzu (Pueraria phaseoloides), and an Opuntia species. The confirmation of the eradication of a blackberry species (Rubus megalococcus) is pending.

Regarding the means by which they arrived in the islands, 825 species (52%) arrived accidentally as contaminants or stowaways, and 724 species (46%) were introduced intentionally. For 2% of the species, the introduction pathway is unknown or questionable (Table 1).

Introduced species currently established in the Galapagos

There are 1476 introduced species that have been reported as established in Galapagos: 810 terrestrial plant species (including varieties and cultivars); 499 insect species; 70 species of other terrestrial invertebrates; 63 pathogens; 27 vertebrate species, including a fish found in coastal lagoons; five marine invertebrate species, and two marine plants.

Of the species established in Galapagos, 868 (58.8%) are naturalized with self-sustaining populations, with insects (467) and terrestrial plants (270) the main taxonomic groups (Table 1). Approximately 37.2% (549) are human-dependent or restricted to human settlements and there is no evidence of dispersal to areas of the Galapagos National Park. Of these, most are terrestrial plants (534). Additionally, 2.3% of the species are possibly exclusively associated with introduced species. The status of 1.7% of the species has not been determined (Table 1).

Discussion

The actual number of species introduced in Galapagos is likely to be higher than the number currently reported due to the following factors:

1. Not all the results from taxonomic and species reviews published in the last five years have been entered into CDF’s Datazone. This is especially true for new reports of introduced insects and microorganisms.

2. Preliminary results from marine habitat censuses

suggest that there are more introduced species than currently reported.

3. Some groups of organisms have not been surveyed adequately, for example Hymenoptera (e.g., microwasps) and soil organisms.

4. There are specimens awaiting identification.

5. There are about 50 plant species whose status is currently unknown; they could either be native or introduced (a pollen or sediment analysis is required for confirmation);

6. Data on interceptions made by inspectors of the

Galapagos Inspection and Quarantine System (SICGAL – Spanish acronym), the organization responsible for quarantine prior to the establishment in 2012 of the Galapagos Biosecurity Agency (ABG – Spanish acronym), have not been included.

Recommendations

1. Merge all introduced species data into a single database, which will enable:

a) A continuously updated checklist and updated taxonomic collection in a single site, thus facilitating scientific research;

b) Introduced species list accessible to all users;

c) Continuous contribution by institutions with information on introduced species.

2. Establish a protocol for all institutions regarding the collection and processing of introduced species data and their introduction pathways to Galapagos. This should have a standard format that facilitates the entry and subsequent use of this data.

3. Publish an annual report updating the number and status of species introduced to the Galapagos Islands.

Acknowledgements

This evaluation would not have been possible without the help of Leon Baert, Sharon Deem, Diana Flores, Anne Guézou, Brand Phillips, Víctor Carrión, Henri Herrera, Patricia Jaramillo, Gustavo Jiménez, Inti Keith, Patricia Parker, Brad Sinclair, Alan Tye, Mónica Ramos, Marcelo Montesdeoca, Nancy Duran, Alex Fonseca, Marco Echeverría, Duglas Acuria, Rafael Conde, Rommel Iturbide, Ronal Azuero, Viviana Duque, Alberto Vélez and other technicians at ABG. We also thank GNPD for their continual support.

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Convention of Biological Diversity (CBD). 2014. Pathways of introduction of invasive species, their prioritization and management. Note by the Executive Secretary. Montreal, 23-28 June 2014.

Hulme PE, S Bacher, M Kenis, S Klotz, I Kühn, D Minchin, W Nentwig, S Olenin, V Panov, J Pergl, P Pyšek P, A Roques, D Sol, W Solarz & M Vilà. 2008. Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology 45:403-414. doi: 10.1111/j.1365-2664.2007.01442.x.

Richardson DM, P Pyšek, M Rejmánek, MG Barbour, FD Panetta & CJ West. 2000. Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6:93-107. doi:10.1046/j.1472-4642.2000.00083.

Toral-Granda MV, Causton CE, Jager H, Trueman M, Izurieta JC, Araujo E, Cruz M, Zander KK, Izurieta A & ST Garnett. 2017. Alien species pathways to the Galapagos Islands, Ecuador. PLOS ONE 12(9): e0184379.

Table 1. Number of species introduced and intercepted in the Galapagos Islands, their current status and pathway of introduction. Status: naturalized (reproduces and propagates itself in the wild without human intervention, as defined by Richardson et al., 2000); human dependent (can only reproduce with human help and / or restricted to human settlements); coexists with introduced species (exclusively associated with introduced species, not necessarily restricted to human settlements); present but status not determined; eradicated (organism eliminated from Archipelago through deliberate intervention); historical record (known only from publications with no current record); intercepted (organism seized in biosecurity procedures and destroyed or returned to mainland Ecuador). Pathway: intentional (brought in on purpose by humans); accidental: contaminant (arrived in goods, animals, plants, etc.); accidental: stowaway (arrived in transport vehicle, cargo, suitcases, etc.); and unknown.

Status in Galapagos

Established

Naturalized 5 2 38 467 68 270 18 868

Human dependent 7 534 8 549

Coexists with introduced species 17 15 2 34

Present but status not determined 8 10 6 1 25

Total number of introduced species established in Galapagos 5 2 63 499 70 810 27 1476

Absent

Eradicated 2 2 4

Historical record 1 8 8 17

Intercepted 15 38 7 9 13 82

Total number of introduced and intercepted species (including absent species) 21 2 63 545 77 821 50 1579

Introduction pathway

Intentional 1 1 1 691 30 724

Accidental: contaminant 63 428 52 127 670

Accidental: stowaway 19 2 97 19 18 155

Unknown 1 19 5 3 2 30

Total number of introduced and intercepted species (including absent species) 21 2 63 545 77 821 50 1579

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BIODIVERSITY AND ECOSYSTEM RESTORATION...and other dominant invaders, such as sauco (Cestrum auriculatum) and wandering jew (Tradescantia fluminensis; Figure 1). Of the 34 plots, 17