BIODIVERSITY AND ECOSYSTEM RESTORATION ä

ä GALAPAGOS REPORT 2015 - 2016

Restoration of the blackberry-invaded Scalesia forest: Impacts on the vegetation, invertebrates, and birds Heinke Jäger1, Sascha Buchholz2, Arno Cimadom3, Sabine Tebbich3, Jacqueline Rodríguez1, Denisse Barrera1, Anna Walentowitz4, Mareike Breuer2, Alonso Carrión5, Christian Sevilla5 and Charlotte Causton1 Photo: © Steven Frank 1Charles Darwin Foundation 2Technische Universität Berlin, Germany 3University of Vienna, Austria 4University of Greifswald, Germany 5Galapagos National Park Directorate

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 Controlled Area were first cut down manually using a study areas at Los Gemelos, and, in 2014, established 34 machete and after two months the regrowth was sprayed permanent 10×10 m plots. All plots contained blackberry with herbicides (applying a mixture of glyphosate and and other dominant invaders, such as sauco (Cestrum Combo©). After another two months, re-sprouting auriculatum) and wandering jew (Tradescantia fluminensis; invasive species were removed by a weed whacker and Figure 1). Of the 34 plots, 17 were within an 8-ha area by hand. Monitoring of the vegetation, invertebrates, and that was left untouched (referred to as the Reference birds was carried out once before control measures were Area), and 17 were within a 6-ha area where blackberry applied, and then again in 2015 and 2016. was controlled (Controlled Area). Invasive plants in the

Los Gemelos

Controlled Area

Reference Area

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 facilitate the germination and/or growth of blackberry.

Plants Percent cover of the non-dominant plant species (herbs, grasses, shrubs, and trees) also increased after chemical Control measures were successful in reducing blackberry control of blackberry (Figure 2), which could be an cover; however, blackberry cover also decreased, though indication of recovery. However, the number of non- to a lesser degree, in the Reference Area over the same dominant introduced species and species of unknown period (Figure 2). This may be because blackberry goes origin increased after control actions were carried out through a natural die-back cycle and then recovers again (Figure 3 A, D) and could have accounted for a higher (H Jäger, pers. observ.). Wandering jew and sauco cover total plant cover. At the same time, total number of increased in the Controlled Area and it is probable that species remained roughly the same, whereas the total the presence of these species suppresses germination number of endemic species slightly decreased (Figure and/or growth of blackberry. Because of this, it might be 3 B, C). This trend was not observed in the Reference beneficial to leave them in areas that they have invaded. Area (Figure 3 A-D) indicating that disturbance caused Although these are also invasive species with a potential by the control measures might have facilitated the negative impact on the surrounding vegetation, they are expansion of invasive species and establishment of other less harmful than blackberry and their removal seems to introduced species, as was also shown in the case of

144 GALAPAGOS REPORT 2015 - 2016 quinine control (Jäger et al., 2009; Jäger & Kowarik, 2010). of Santa Cruz during February 2016. No new seedlings Future monitoring is needed to show whether this is an were found in this area. During the same time, 47 out of ephemeral phenomenon or not. 255 (18.4%) trees died in the Controlled Area; however, the chemical control of blackberry had a spectacular Percent cover of Scalesia pedunculata in the Reference Area effect on the regeneration of Scalesia pedunculata. Only decreased by a third over the monitoring period (Figure 2 five months after the last herbicide application by the A), which could be due to tree mortality. Over the course of GNPD, up to 280 Scalesia seedlings per plot were found two years, 71 out of 200 (35.5%) trees died in the Reference at the Controlled Area where there had been none during Area. The reason for this is not clear but could have been our first monitoring. This was reflected by an increase in caused by strong winds that occurred in the highlands Scalesia cover in the Controlled Area (Figure 2 B).

200 200 2014 2016 150 150

100 100 % Cover % Cover

50 50

0 0 no dom Ces_aur Rub_niv Tra_ u Sca_ped no dom Ces_aur Rub_niv Tra_ u Sca_ped

Reference Area Controlled Area

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).

30 30 A B Reference Area 25 25 Controlled Area 20 20

15 15

10 10 Total #NaQ species Total

5 species # native Total 5

0 0 2014 2014 2014 2014

30 30 C D 25 25

20 20

15 15

10 10

5 5 Total # endemic species Total Total # introduced species # introduced Total 0 0 2014 2014 2014 2014 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).

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We also determined that the threshold of blackberry Analyses at species level are pending. At this stage, it cover that the resident plant species (native and endemic) is difficult to reach conclusions about the dynamics can tolerate, and under which they can still thrive, is about of invertebrates in both study areas. Preliminary data 60%. These results confirm those of Rentería et al. (2012), on spider abundance (Araneae) showed similar trends who also determined a 60% blackberry cover as (barely) in the Reference Area and Controlled Area (Figure 4), tolerable for the persistence of the resident plant species suggesting that climate might influence invertebrate in the understory. While this percentage is far from ideal, it numbers at both sites. However, this does not explain the can serve as a guideline for management actions. difference in abundance between the two study areas prior to and after control efforts. Further analyses and Invertebrates continued monitoring are needed to determine whether management efforts have affected invertebrate diversity Around 16,184 specimens were collected from Malaise and abundance. traps and 766 from Pitfall traps set out in the study areas.

Reference Area Controlled Area 250 250

200 200

150 150

100 100 Total # Spiders Total # Spiders Total 50 50

0 0 2014 2015 2016 2014 2015 2016 Malaise traps Pitfall traps

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).

Birds area before and after the control measures was influenced by drought conditions in 2015. Breeding success in this The breeding success of the green warbler-finch and small year was extremely low for both species in both areas. The tree-finch did not differ significantly between the two areas overall very low breeding success may have masked the in any of the three years (Figure 5). The comparison within short-term effect of the mechanical and chemical control

60 60 Reference Area Controlled Area 50 50

40 40

30 30

20 20

10 10 % Successfull nests Warbler-Finch nests % Successfull 0 Tree-Finch nests Small % Successfull 0 2014 2015 2016 2014 2015 2016

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

146 GALAPAGOS REPORT 2015 - 2016 that had been observed in previous years (Cimadom et al., To ensure the continued success of this control program, 2014). In 2016, which was the second breeding season after the following management actions are recommended: the control measures, the breeding success of the green warbler-finch was lower in the Controlled Area than in 1. Maintain a long-term monitoring program to evaluate the Reference Area, indicating a negative effect of habitat blackberry control methods and results. management. Breeding success of the small tree-finch was extremely low in both areas throughout the study. 2. Do not control sauco and wandering jew in the protected areas as their presence tends to help We found no significant detrimental (negative) effect of suppress blackberry. invasive plant management on bird numbers. Bird counts showed a slight increase of singing males per point in 3. Maintain the cover of blackberry at 60% or less to 2015 and 2016 compared to 2014 in most species in both ensure survival of surrounding vegetation. areas. The only pronounced change was an increase in the number of small ground-finches in the Controlled Area in 4. Continuously remove blackberry seedlings by hand- 2015, right after the implementation of control measures. pulling from areas that have been controlled, as This species seems to move into the open areas created by blackberry regenerates vigorously from seeds. the removal of the understory. 5. Analyze herbicide residuals in soil and water samples Conclusions and Recommendations at Los Gemelos to assess contamination.

Long-term monitoring will reveal more about how animal Acknowledgements and plant communities respond to blackberry removal. In the meantime, preliminary results indicate that methods We would like to acknowledge the financial support to control blackberry are effective and that blackberry by Galapagos Conservancy and Keidanren Nature regeneration can be prevented by other invasive, but less Conservation Fund to carry out the vegetation and detrimental, plants. Regeneration of Scalesia pedunculata invertebrate monitoring. We are also very grateful for was only possible in blackberry-controlled areas and the hard work of the GNPD park rangers who made this was very high, suggesting that interventions to control study possible. The bird monitoring was supported by a this invasive plant are needed. However, the continuous FWF-grant from the Austrian Government. Furthermore, germination of blackberry seeds in the Controlled Area we would like to thank the numerous local, national, requires follow-up removal of blackberry seedlings for and international field assistants for their help in data several years after intervention. collection and processing.

References Cimadom 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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Galapagos landbirds (passerines, cuckoos, and doves): Status, threats, and knowledge gaps Photo: © David Anchundia Birgit 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 Foundation 2Galapagos National Park Directorate 3Universiy of Vienna, Austria 4 BirdLife Austria 5 Frohnatur Austria

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).

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

In response to the declines in some landbird populations, it will be possible to detect and respond to population the Charles Darwin Foundation (CDF) and the Galapagos changes. Here we provide an overview of the surveys National Park Directorate (GNPD), in collaboration conducted on the four inhabited islands and Santiago with a group of ornithologists, developed a landbird within the past six years, and identify factors that may be conservation plan (Cunninghame et al., 2012). This plan responsible for the decline of some species. 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,

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).

Islands with IUCN-status2 Distribution and habitat type knowledge gaps Species name1 Origin (E, N, I)3 Known host for Philornis downsi Options for citizen science Number of subspecies [ ] (CS) Common; on all main islands except Small ground-finch Genovesa, Darwin, and Wolf. LC, stable, E None Geospiza fuliginosa All vegetation zones. Host of P. downsi. Common; on all main islands except Genovesa, Medium ground-finch At risk on Floreana, more LC, stable, E Española, Darwin, and Wolf. Geospiza fortis studies needed Host of P. downsi. Present on all islands except Española and Darwin. All islands; habitat prefer- ence not completely Extinct on Floreana and San Cristóbal. understood; very patchy distribution on Santa Cruz Large ground-finch LC, stable, E and possibly all other Geospiza magnirostris Lowlands. larger islands. Difficult to get Host of P. downsi. valuable density data with currently applied counting methods. CS

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

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Occurs in highland forest on Santiago, Fernandina and Pinta. Sharp-beaked ground-finchA LC, stable, E Extinct on Santa Cruz, San Cristóbal, Floreana, and Pinta, Fernandina. CS Geospiza difficilis probably Isabela. Studies on P. downsi missing.

Genovesa ground-finchA VU (classified as a species in Genovesa. Genovesa Geospiza acutirostris 2016), stable, E P. downsi not reported for Genovesa.

Vampire ground-finchA VU (classified as a species in Darwin and Wolf. Geospiza septentrionalis 2016), stable, E P. downsi not reported for Darwin and Wolf.

Present on all main islands except Fernandina, Española, Genovesa, Darwin, and Wolf. Extinct on Pinzón. Common cactus-finch Floreana, San Cristóbal, LC, stable, E [4] Geospiza scandens Apparently very rare on San Cristóbal Isabela, Santiago. CS (few records during surveys). Arid zone with cacti. Host of P. downsi.

Believed to be common on Española. Española ground-finchB VU ( classified as a species Arid zone with cacti. Española Geospiza conirostris in 2016), stable, E P. downsi not reported for Española.

Genovesa cactus-finchB VU (classified as a species Believed to be common on Genovesa. Genovesa Geospiza propingua in 2016), stable, E P. downsi not reported for Genovesa.

Present on all main islands except Santa Fe, All uninhabited islands Genovesa, Española, Darwin, and Wolf. except Santiago highlands. Vegetarian finch LC, stable, E Possibly extinct on Floreana. Little is known about this Platyspiza crassirostris species; an ecological study Arid and transition zones. would be worthwhile. Host of P. downsi. Present on all main islands except Marchena, Small tree-finch Genovesa, Española, Darwin, and Wolf. All uninhabited islands LC, stable, E [2] Camarhynchus parvulus Highlands; lower densities in lowlands. except Santiago highlands. Host of P. downsi. Floreana; the population is larger than previously thought and seems stable but breeding success is Long-term study ongoing Medium tree-finch CR (since 2009), possibly low. (S Kleindorfer, Flinders Camarhynchus pauper decreasing, E Highland forest. University, Australia). Host of P. downsi. Present on all main islands except San Cristóbal, Fernandina, Isabela Española, Genovesa, Darwin, and Wolf. volcanoes, Pinta, Marchena, Extinct (if ever permanently present) on Floreana. Rábida, Santiago, Pinzón, and Santa Fe. Large tree-finch VU (since 2015), Low densities on Santa Cruz and Genetic studies on Camarhynchus psittacula decreasing, E [3] Sierra Negra Volcano, Isabela. differences among islands No quantitative data from all other islands necessary to evaluate status and possibly severely threatened. of currently described Highland and transition forest. subspecies. Host of P. downsi. Present on Isabela, Santiago, Santa Cruz and San Cristóbal. Genetic, morphological, Possibly occurring (single specimens or and ecological studies on differences between islands Woodpecker finch VU (since 2015), unconfirmed sight records) on Pinta, Fernandina, in progress (E Nemeth & M Camarhynchus pallidus decreasing, E [3] Pinzón, Rábida, and Santa Fe. Dvorak, BirdLife Austria). Confirmation of doubtful Highlands; very low densities in arid zones. island occurrences. 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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Isabela and Fernandina. Some known hybridization with the woodpecker finch. This species is currently under Mangrove finch CR (since 2000), Mangrove forest. At the moment only breeding intensive management by the Camarhynchus heliobates decreasing, E population north of Tagus Cove. Mangrove Finch Project (GNPD & CDF). Continuous funding and support needed to keep the Host of P. downsi. species viable.

Isabela, Santa Cruz, Fernandina, Santiago, Green warbler-finch LC (classified as a species Pinzón, and Rábida. Fernandina, Pinzón, Rábida, and Certhidea olivacea in 2016), stable, E Highland zones into transition zone. Isabela except Sierra Negra. Host of P. downsi. San Cristóbal, Marchena, Española, Pinta, Santa Fe, and Genovesa. Marchena, Pinta, Santa Fe, Española, and Genovesa. Gray warbler-finch LC (classified as a species Extinct on Floreana. Clarify taxonomic status of birds Certhidea fusca in 2016), stable E [6] Inhabits dry zone on most islands; in San Cristóbal from San Cristóbal. known from transition zone up into the highlands. Studies on P. downsi missing.

LC, stable, N (endemic Yellow warbler All main islands and all habitat types. All uninhabited islands except subspecies for Galapa- Setophaga petechia Host of P. downsi. Santiago highlands. gos and Cocos Island)

All main islands except Genovesa, Española, and Baltra.

Probably extinct from Floreana. All islands. CS. Little vermilion flycatcher* VU (classified as a species Nest success study at El Cura, Pyrocephalus nanus in 2016), decreasing, E Rare on Santa Cruz and Santiago. Sierra Negra, Isabela in progress (CDF). On some islands only in highlands and transition zones; on small islands also known from the lowlands. Host of P. downsi. Recent surveys (2015-2016) Least vermilion flycatcher EX (classified as a species unsuccessful in finding species. San Cristóbal; last seen in 2008. Pyrocephalus dubius in 2016) Searches in very remote areas needed to confirm status. Present on all islands except Genovesa, Galapagos flycatcher Darwin, and Wolf. All uninhabited islands except LC, stable, E Myiarchus magnirostris Lower numbers in highlands. Santiago highlands. Host of P. downsi.

Present on all main islands without island-specific species. Galapagos mockingbird Fernandina, Marchena, and LC, stable, E [6] More common in lowlands. Lower numbers in Mimus parvulus Santa Fe. CS. highlands. Host of P. downsi.

This species is currently under Extinct on Floreana. care of the Floreana Mocking- bird Project (GNPD and Massey Floreana mockingbird CR (since 2008), E University, New Zealand). No Mimus trifasciatus Small remnant populations on two islets (Champion & Gardner) close to Floreana. management needed so far as Host of P. downsi. populations appear stable (L. Ortiz-Catedral, pers. comm.).

No information on status; Española mockingbird Española. VU (since 2008), E systematic population survey Mimus macdonaldi P. downsi not reported for Española. necessary.

San Cristóbal. Arid zone on San Cristóbal, San Cristóbal mockingbird EN (since 2006), E Common in all habitats. especially outside easily Coccyzus melacoryphus Host of P. downsi. accessible sites. CS.

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

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All uninhabited islands. Little to nothing is known about this species (including Dark-billed cuckoo All main islands and all habitat types. genetics). LC, stable, N Coccyzus melacoryphus Host of P. downsi. Calling activity highly variable between years, therefore difficult to obtain reliable population estimates. CS.

All main islands and all habitat types. All uninhabited islands. Has Very rare on San Cristóbal, Floreana and patchy become very rare on inhabited Galapagos dove LC, stable, E [2] distribution on Santa Cruz. islands, thus special attention Zenaida galapagensis needed to look at factors Studies on P. downsi missing. causing decline. CS.

Present in low numbers on all islands. Unobserved All islands. from Marchena, Genovesa, Pinta, Darwin, and Wolf. This species needs a special Galapagos martin* EN (since 2008), E program to be properly Progne modesta Needs cliffs for nesting. assessed. CS. Studies on P. downsi missing. Present on all main islands. All islands. Status on Fernandina unknown. Smooth-billed ani Reports from all islands other LC, stable, I Eradicated from Marchena. Crotophaga ani than inhabited ones needed to All habitat types. assess distribution. CS. Host of P. downsi.

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

Bird population surveys Floreana

For the first time we have baseline data for all passerine Pirates and whalers were impacting the flora and fauna species and most other landbirds from San Cristóbal, before the first human settlement in 1832. Furthermore, Floreana, Santa Cruz, the highlands of Santiago, and Sierra the effects of introduced mammals (e.g., cattle, goats, Negra volcano on Isabela (Table 2). donkeys, and cats) were more severe on Floreana than on other Galapagos Islands (Steadman, 1986), probably San Cristóbal leading to the disappearance of the Floreana mockingbird (Mimus trifasciatus) now confined to two small satellite This is the oldest island of the Archipelago and the islands (Steadman, 1986; Jiménez-Uzcátegui et al., only one with running fresh water. Permanent human 2011), and the sharp-beaked ground-finch, now extinct settlements began in 1837; current population is (Sulloway, 1982). Today, the human population numbers estimated at 7500 residents (INEC, 2010). While natural about 150. Floreana is home to one of the largest vegetation remains in the lowlands, there is little native preserved endemic highland Scalesia forests in the vegetation left in the humid highland zone as a result of Archipelago. Nevertheless, during our counts we recorded intensive agriculture (Watson et al., 2010). Of the 11 small no vermilion flycatchers, large tree-finches, gray warbler- landbird species that were collected and mentioned by finches (subspecies Certhidea fusca ridwayi), or vegetarian Swarth (1931), the vermilion flycatcher (last seen in 2008) finches. The first three species were already suspected to was missing in the recent survey; the Galapagos dove be extinct (Grant et al., 2005; Merlen, 2013; Kleindorfer and the common cactus-finch were very rare. The latter et al., 2014a), while the absence of the vegetarian finch, two might be more common in unsurveyed parts of the formerly common (47 specimens collected in 1905/06; arid zone. Swarth, 1931), was unexpected. The most recent records of vegetarian finches are from 1962, by R. Bowman (www. The introduced smooth-billed ani, encountered in all macaulay-library.org), 2004 (Grant et al., 2005), and 2008 habitat types, was rare in the arid zone. The population of (O’Connor et al., 2010c). The Galapagos dove was only the endangered San Cristóbal mockingbird, encountered found at two sites in the highlands and one site in the in all vegetation zones, is several times larger (10-15,000 lowlands; it may still exist in remote areas of the arid breeding pairs) than the 8000 individuals estimated in zone. Lastly, the medium ground-finch and the common 2005 (IUCN, 2016). 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.

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

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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.

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

Sierra Negra, 2015 (CDF/GNPD landbird project), Alcedo, Cerro Azul, Darwin, Wolf, and lowlands Isabela 4588 Playa Tortuga Negra since 2006, Wolf Volcano 2015 including Pto. Villamil, Sierra Negra (landbird project) / P. downsi present

Multiple years since 1996 (Dvorak et al., 2012), last Northern arid zone Santa Cruz 986 comprehensive survey 2014 (Dvorak, Nemeth & Wendelin) / P. downsi present Scalesia: every breeding season Other habitat zones: every 3-5 years Highlands: important for assessment of the Fernandina 642 P. downsi present sharp-beaked ground-finch and other tree finches

Lowlands and transition zone forest Highlands in 2016 Santiago 585 (CDF/GNPD landbird project) / P. downsi present Highlands should be repeated in 3-5 years

Additional sites in the dry zone and very remote areas for the vermilion flycatcher Lowlands 2010 (Dvorak & Nemeth), island-wide San Cristóbal 558 (in cooperation with GNPD) 2015 (landbird project) / P. downsi present Highlands: every 3-5 years

2004, 2008, 2011 (highlands, Kleindorfer et al.); 2010 Floreana 173 & 2014 (highlands, Dvorak & Nemeth); 2015 & 2016 Repeat survey in 3-5 years (island-wide, landbird project) / P. downsi present

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

Island without any identified threats or endangered species (other than Española Española 60 2010 (CDF) / P. downsi absent mockingbird). However, recent authorization of day-tours makes baseline monitoring fundamental. Important for assessment of the sharp-beaked Pinta 60 2014 (Keller et al.) / P. downsi present ground-finch, woodpecker finch, and large tree-finch Lowest priority; island with cat eradication, 2014 (UCSC-CCAL, outside breeding season) no endangered species; assessment of Baltra 27 / P. downsi present 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

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

Island without any identified threats; 1973, 1978-1988 (Grant et al.); 2014 (Keller et al.) Genovesa 14 assessment of sharp-beaked ground-finch, / P. downsi absent large ground-finch. and large cactus-finch

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

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

On the other hand, our population estimate of 3900-4700 the majority of the breeding population inhabits farmland territories for the medium tree-finch is considerably higher and abandoned farmland, now part of the Galapagos than the previous estimate of 1620 males (O’Connor et al., National Park, characterized by a mixture of introduced 2010a). Our monitoring data provide the most accurate and native vegetation with high trees (mainly Cedrela delimitation of the breeding range of this species, odorata) (Dvorak et al., unpubl. data). showing that it is not confined to the Scalesia forest but

154 GALAPAGOS REPORT 2015 - 2016

The smooth-billed ani is common in all ecological zones. green warbler-finch, woodpecker finch, yellow warbler, and vermilion flycatcher. Monitoring data (2008-2015) Agricultural and fern zone of Sierra Negra from the arid, agricultural, and fern zones showed that Volcano, Isabela for some species and habitat types, the observed decline has not continued, with numbers seeming to stabilize The forested highlands (agricultural and park area) are around the lower values calculated in 2008. Counts from covered by secondary vegetation, mainly guava (Psidium the remaining Scalesia habitat are highly variable. The guajava) and Ecuadorian walnut (Juglans neotropica). green warbler-finch continues to decline in this fragile Our bird surveys in 2015 provide the first estimates of forest as in the fern zone, its two remaining strongholds. landbird distribution and abundance for this area. The The small tree-finch, seemingly stable between 1997 and small ground-finch, small tree-finch, green warbler-finch, 2008, is now decreasing in the highlands. Large tree-finch woodpecker finch, and yellow warbler are common, while numbers are low; this species needs special attention the large tree-finch is restricted to areas with high trees in the future. Galapagos doves, formerly common, are only. The vermilion flycatcher is widespread and common now rare especially around inhabited areas, but might in El Cura at an elevation between 550 and 1050 m (D have refuges in the northern arid zone where few counts Mosquera, unpubl. data). They seem to prefer older guava have been conducted. Vermilion flycatchers are now so forests or stands where farmers have removed the dense rare that they cannot be assessed with the point count understory. Density is lower at decreasing elevations method. According to specific searches done in 2015, the and may be associated with clearing of guava stands, population estimate is around 30 to 40 breeding pairs with deserving special attention in the future. core zones north of El Puntudo and north of Los Gemelos around the red gravel mine. Ground finches are expanding Santiago further into the highlands, probably due to an increase in open habitat and many introduced small herb species now This currently uninhabited island was historically a source present in the Scalesia and fern zones, providing a seed of fresh water, wood, and tortoises for buccaneers and source. Smooth-billed anis are encountered throughout whalers. In the 1920s and 1960s, salt was extracted the island, though numbers have declined since 2008, commercially. Goats, pigs, and donkeys were released probably due to control measures by the GNPD. in the early 1800s and changed the highland zone considerably, though vegetation is recovering since their Principal reasons for population declines and successful eradication (Cruz et al., 2005; Carrión et al., 2007; recommended priority actions Cruz et al., 2009). All landbird species noted by Swarth (1931) were recorded in our survey in 2016, which focused Threat 1 – Philornis downsi on the highlands. The sharp-beaked ground-finch was widely distributed, but occurred only in comparatively In the late 1990s, a highly invasive parasitic fly, P. low densities. The vermilion flycatcher and large tree-finch downsi, was found to be significantly impacting were encountered only at one site each in transition forest reproductive output of most small landbirds dominated by Galapagos guava (Psidium galapageium). A (reviewed in Kleindorfer et al., 2014b). This fly is found thorough search is necessary to further clarify the status throughout the Archipelago (Table 2) affecting many of these species. The island has a healthy population of landbird species (Table 1). P. downsi is classified as one Galapagos doves, with birds observed in all habitat types. of the most invasive species in Galapagos (Causton They were frequently seen digging into the abundant et al., 2006) and is the most serious threat for many tortoise dung searching for food. landbirds. Parasite-induced nestling mortality is high. Beak and naris deformation persisting into adulthood Santa Cruz (Galligan & Kleindorfer, 2009) can affect courtship (birds sing differently) or make birds vulnerable during Since the 1980s, Santa Cruz Island, settled in 1920, has had times of food scarcity. the highest human population (currently >15,000) and the highest population growth (Epler, 2007; INEC, 2006; Actions. Research on the biology and ecology of P. INEC, 2010). The endemic Scalesia forest is reduced to 1% downsi must continue to find methods to reduce fly of its former extent (Mauchamp & Atkinson, 2011) and populations and protect landbirds. The international the highlands are heavily invaded by blackberry (Rubus Philornis working group, comprising 20 institutions niveus), quinine (Cinchona pubescens), and invasive herbs from eight countries, is evaluating potential short- (Jäger et al., 2009; Jäger et al., this volume). This is the only term control methods, such as in situ nest treatment island where some long-term landbird monitoring has and fly trapping, until low-risk methods for permanent been carried out. A comparison of bird counts between suppression of P. downsi over large areas are developed. 1997 and 2008 revealed that six of nine surveyed species Potential methods include biological control using had seriously declined (Dvorak et al., 2012; Figure 2). Of natural enemies and the Sterile Insect Technique. these, five are insectivorous species: large tree-finch,

155 GALAPAGOS REPORT 2015 - 2016

Arid Transition Farmland Scalesia Fern 1997 - 2008 - 1997 - 2008 - 1997 - 2008 - 1997 - 2008 - 1997 - 2008 - 2008 2014-15 2008 2014-15 2008 2014-15 2008 2014-15 2008 2014-15 Small ground-finch SSSSVVVVSI Medium ground-finch ISSSSV IR VAI Common cactus-finch SSAAAAAAAA Vegetarian finch SSSSDS IR IR AA Small tree-finch SSSSSDSVSS Large tree-finch DDSSVVSVAA Woodpecker finch DSSSDSDVSS Green warbler-finch IR IR DSDSDDSD Yellow warbler DSVDDSVVDI

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 Galapagos with higher incidences on inhabited islands (Kilpatrick et al., 2006; Deem et al., 2011; Parker et al., In Galapagos, introduced rodents and cats (Felis 2011). Several strains of Plasmodium were identified in silvestris) are known bird predators (Fessl et al., 2010a; Galapagos (Levin et al., 2013). Pathogens can impact Harper & Carrión, 2011; Konecny, 1987); while cats only passerine survival and even lead to extinction (Van occur on inhabited islands, black rats (Rattus rattus) Riper et al., 1986; Dunn et al., 2013). The most important and mice (Mus musculus) are widespread (Phillips et al., challenge for Galapagos is the prevention of future 2002). No significant rat predation on landbird nests introductions. was observed in the highland Scalesia forest (O’Connor et al., 2010b - Floreana; Cimadom et al., 2014 – Santa Actions. Baseline health monitoring including Cruz), but heavy predation by black rats has been monitoring of avian pox is well underway for many observed in the lowlands of Floreana (O’Connor et bird species (Parker & Deem, 2012). The collaborative al., 2010b) and on mangrove finch nests (Fessl et al., project between University of Missouri, Wild Care 2010b). Impacts of mice or the introduced smooth- Institute Saint Louis Zoo, GNPD, and CDF to collect billed ani — a potential predator, disease vector, and baseline data on blood parasites needs to be continued food competitor — are largely unknown. and expanded. Protocols for avian disease prevention need to be developed and efforts to reduce mosquito Actions. Rat, cat, and smooth-billed ani monitoring vectors need to be supported as much as possible. and control are important for threatened native and endemic birds. On inhabited islands, increased efforts Threat 4 – Habitat degradation to decrease rat and cat populations are important in particular in agricultural areas, which are key Major habitat changes have occurred on inhabited habitats for some tree finch species. Expanding the islands because of human settlements and on cat sterilization program would help reduce cat uninhabited islands due to introduced herbivores. populations. A better understanding of the ecology Almost all humid highland forests on inhabited islands of the smooth-billed ani will help determine the need were cleared for agriculture. The humid Scalesia forest, and feasibility of an eradication plan. Currently, Sophia a prime habitat for tree finches, is a fraction of its Cooke (Cambridge University), with CDF and GNPD, is original extension on Santa Cruz, Santiago, southern studying its ecology, and developing different trapping Isabela, and San Cristóbal. Herbicide use to control designs for a targeted removal of smooth-billed anis. invasive plants may have secondary impacts on landbirds through reduced food availability (Jäger et Threat 3 – Diseases and disease vectors al., this volume; Cimadom et al., 2014), while pesticides may also be affecting native birds (Hallmann et al., Diseases (e.g., avian pox) and animals that are 2014). potential disease vectors (e.g., the mosquito Culex quinquefasciatus, potential vector of avian malaria, Actions. The protection and restoration of the last and cats, vectors of Toxoplasma) are now present in remnants of Scalesia forest on Santa Cruz, San Cristóbal,

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and Floreana Islands have highest priority. The combined with natural population fluctuations caused agricultural zones are refuges for several bird species, by stressors such as climatic extremes they can seriously and efforts should focus on encouraging bird-friendly affect nesting success, survival (Cimadom et al., 2014; agricultural practices with minimal use of eco-friendly Koop et al., 2015), and recruitment. For example, habitat herbicides and insecticides, and habitat management, alteration can lead to reduction in food for birds that are e.g., the replanting of native trees, especially Scalesia then less able to compensate for the effects of parasitism and Galapagos guava. Incentive schemes could by P. downsi. It is important to understand the impact of be implemented such as the Bird Friendly Seal of the different factors on birds and the interactions between Approval (Smithsonian Migratory Bird Center) or them in order to develop and implement management special recognition given to farms that protect nesting actions to prevent further losses. sites of native species. Data presented from Santa Cruz show the importance An action plan and protection of the last refuges of of long-term monitoring to detect bird population the vermilion flycatcher on Santa Cruz are urgently changes. The aim over the next few years is to establish needed and should include control of P. downsi, an institutional long-term monitoring program for all rodents, cats, and the invasive blackberry (without the islands >5 km2 in size, with special focus on islands with use of herbicides). A management plan is also needed single island endemics or small, distinct populations. As for El Cura on southern Isabela, where the vermilion all quantitative counting methods need specially trained flycatcher prefers old guava stands; guava removal personal, the involvement of Ecuadorian ornithologists in from the park area would highly impact the population. monitoring programs must be expanded. A long-term plan for the replacement of guava by less invasive trees is needed. Lastly, an impact study of Citizen science can and should help for easy-to-recognize currently used pesticides on invertebrate communities species (Table 1). Together with the company “Birds in and bird health is needed. the Hands”, LLC, we have developed a free Galapagos Bird App that provides pictures and information to help Threat 5 – Road kill in bird identification. This app will be promoted, and residents, tourists, naturalist guides, and park rangers A census conducted by the GNPD on Santa Cruz in 2013 invited to report bird sightings via eBird. A program has (Los Gemelos to Canal Itabaca) revealed that during already been initiated with some tour operators to get three months (breeding season) more than 1000 birds site-specific data for birds with important knowledge were killed, 90% of which were yellow warblers. Short- gaps, such as the Galapagos martin. In conjunction with eared owls (Asio flammeus) and barn owls (Tyto alba) a professionally led monitoring program, we hope to have also been found killed regularly (A. Carrión, pers. collect usable data and, at the same time, raise awareness com.). The impact of road kill on bird communities and increase local involvement. overall is unknown. Acknowledgments Actions. We need to investigate the impact of road kills on populations of the most affected species. More The Galapagos Landbird Plan, implemented jointly by the speed bumps or section control units are needed in Charles Darwin Foundation and the Galapagos National critical areas, especially in the section through Los Park Directorate, is funded by Galapagos Conservancy Gemelos to Canal Itabaca. In the long-term, a more and the International Community Foundation (with a ecological transport system, favoring buses to the grant awarded by The Leona M. and Harry B. Helmsley canal, should be sought for Santa Cruz. Charitable Trust). Fieldwork on Floreana was partially funded by Island Conservation. A special thank you to Conclusions Andre Mauchamp for comments on a former draft and help in editing. The threats to landbirds are not mutually exclusive; when

References Callaway R & E Aschehoug. 2000. Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521-523. Carmi O, C Witt, A Jaramillo & J Dumbacher 2016. Phylogeography of the Vermilion Flycatcher species complex: multiple speciation events, shifts in migratory behavior, and an apparent extinction of a Galapagos-endemic bird species. Molecular phylogenetics and evolution 102:152-173. Carrión V, J Donlan, K Campbell, C Lavoie & F Cruz. 2007. Feral donkey (Equus asinus) eradications in the Galapagos. Biodiversity and Conservation 16:437-445.

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Causton C, S Peck, B Sinclair, L Roque-Albedo, C Hodgson & B Landry. 2006. Alien insects: threats and implications for the conservation of the Galapagos Islands. Annals of the Entomological Society of America 99:121-143. Cimadom 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. Cruz F, V Carrión, K Campbell, C Lavoie & C Donlan. 2009. Bio-economics of large-scale eradication of feral goats from Santiago Island, Galapagos. Journal of Wildlife Management 73:191-200. Cruz F, C Donlan, K Campbell & V Carrión. 2005. Conservation action in the Galapagos: feral pig (Sus scrofa) eradication from Santiago Island. Biological Conservation 121:473-478. Cunninghame, L Ortiz-Catedral & B Fessl. 2012. Landbird Conservation Plan: Strategies for reversing the decline of passerine birds on the Galapagos. Fundación Charles Darwin, Dirección del Parque Nacional Galápagos, Puerto Ayora, Galápagos, Ecuador. Deem S, M Cruz, J Higashiguchi & P Parker. 2011. Diseases of poultry and endemic birds in Galapagos: implications for the reintroduction of native species. Animal Conservation 15:73-82. Dunn J, S Goodman, T Benton & K Hamer. 2013. Avian blood parasite infection during the non-breeding season: an overlooked issue in declining populations? B.M.C. Ecology 13:30. Dvorak M, B Fessl, E Nemeth, S Kleindorfer & S Tebbich. 2012. Distribution and abundance of Darwin’s finches and other land birds on Santa Cruz Island, Galapagos: evidence for declining populations. Oryx 46:1-9. Epler B. 2007. Tourism, the Economy, Population, Growth, and Conservation in Galapagos. Fundación Charles Darwin. Farrington H, L Lawson, C Clark & K Petren. 2014. The evolutionary history of Darwin’s finches: speciation, gene flow, and introgression in a fragmented landscape. Evolution 68:2932-2944. Fessl B, H Vargas, V Carrión, R Young, S Deem, J Rodríguez-Matamoros, R Atkinson, C Grenier, O Carvajal, F Cruz, S Tebbich & H Young. 2010a. Galapagos Mangrove Finch Camarhynchus heliobates Recovery Plan 2010-2015. Fideicomiso Durrell para la Conservación de la Vida Silvestre (Durrell Wildlife Conservation Trust), Fundación Charles Darwin, Servicio Parque Nacional Galápagos.

Fessl B, H Young, R Young, J Rodríguez-Matamoros, M Dvorak, S Tebbich & J Fa. 2010b. How to save the rarest Darwin’s finch from extinction: the mangrove finch on Isabela Island. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:1019-1030. Galligan T & S Kleindorfer. 2009. Naris and beak malformation caused by the parasitic fly, Philornis downsi (Diptera: Muscidae), in Darwin’s small ground finch, Geospiza fuliginosa (Passeriformes: Emberizidae). Biological Journal of the Linnean Society 98:577-585. Grant P, B Grant & K Petren. 2000. The allopatric phase of speciation: The sharp-beaked ground finch (Geospiza difficilis) on the Galapagos Islands. Biological Journal of the Linnean Society 69:287-317. Grant P, B Grant, K Petren & L Keller. 2005. Extinction behind our backs: the possible fate of one of the Darwin’s finch species on Isla Floreana, Galapagos. Biological Conservation 122:499-503. Hallmann C, R Foppen, C van Turnhout, H de Kroon & E Jongejans. 2014. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 10.1038/nature13531. Harper G & V Carrión. 2011. Introduced rodents in the Galapagos: colonization, removal and the future. En Turning the tide. The eradication of invasive species (ed C Veitch & M Clout). Pp 63-66. Grupo Especializado en Especies Invasoras de la UICN SSC. Harris M. 1973. The Galapagos avifauna. The Condor 75:265-278. INEC. 2006. Censo Galápagos 2006. Instituto Nacional de Estadísticas y Censos, Quito, Ecuador. INEC. 2010. Fascículo Provincial Galápagos. Resultados del Censo 2010. Instituto Nacional de Estadísticas y Censos, Quito, Ecuador. IUCN. 2016. The IUCN Red List of Threatened Species. Version 2016. . Downloaded 13 March 2017. 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. Jiménez-Uzcátegui G, W Llerena, W Milstead, E Lomas & D Wiedenfeld. 2011. Is the population of Floreana Mockingbird Mimus trifasciatus declining? Cotinga 33:1-7.

158 GALAPAGOS REPORT 2015 - 2016

Kilpatrick A, P Daszak, S Goodman, H Rogg, L Kramer, V Cedeño & A Cunningham. 2006. Predicting pathogen introduction: West Nile Virus spread to Galapagos. Conservation Biology 20:1224-1231. Kleindorfer S, J O’Connor, R Dudaniec, S Myers, J Robertson & F Sulloway. 2014a. Species collapse via hybridization in Darwin’s Tree Finches. The American Naturalist 183:325-341. Kleindorfer S, K Peters, G Custance, R Dudaniec & J O’Connor. 2014b. Changes in Philornis infestation behavior threaten Darwin’s finch survival. Current Zoology 60:542-550. Konecny M. 1987. Food habits and energetics of feral house cats in the Galapagos Islands. Oikos 50:24-32. Koop J, P Kim, S Knutie, F Adler & D Clayton. 2015. An introduced parasitic fly may lead to local extinction of Darwin’ s finch populations. Journal of Applied Ecology 10.1111/1365-12664.12575. Lamichhaney S, J Berglund, M Sällman Almén, K Maqbool, M Grabherr, Martínez-Barrio A, M Promerova, C-J Rubin, C Wang, N Zamani, B Grant, P Grant, M Webster & L Andersson. 2015. Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature 518:371-376. Levin I, P Zwiers, S Deem, E Geest, J Higashiguchi, G Jiménez-Uzcátegui, D Kim, J Morton, N Perlut, T Iezhova, G Jime, R Renfrew, E Sari, G Valkiunas & P Parker. 2013. Multiple Lineages of Avian Malaria Parasites (Plasmodium) in the Galapagos Islands and Evidence for Arrival via Migratory Birds. Conservation Biology 27:1366-1377. Luzuriaga N, F Jiguet, M Gardener, S Véran & P Henry. 2012. Monitoring an endemic community of terrestrial birds: the Galapagos Islands Breeding Bird Survey (GIBBS). Bird Census News 25:3-12. Maron J & M Vilà. 2001. When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361-373. Mauchamp A & R Atkinson. 2011. Rapid, recent and irreversible habitat loss: Scalesia forest on the Galapagos Islands. En Galapagos Report 2009-2010. Pp 108-112. SPNG, CGREG, FCD y GC, Puerto Ayora, Galápagos, Ecuador. Merlen G. 2013. Gone, gone...going: The fate of the vermilion flycatcher on Darwin’s Islands. In Galapagos Report 2011- 2012. Pp 180-188. SPNG, CGREG, FCD y GC. Puerto Ayora, Galápagos, Ecuador.

O’Connor J, R Dudaniec & S Kleindorfer. 2010b. Parasite infestation and predation in Darwin’s small ground finch: contrasting two elevational habitats between islands. Journal of Tropical Ecology 26:285-292. O’Connor J, F Sulloway & S Kleindorfer. 2010c. Avian population survey in the Floreana highlands: Is Darwin’s Medium Tree Finch declining in remnant patches of Scalesia forest? Bird Conservation International 20:1-11. O’Connor J, F Sulloway, J Robertson & S Kleindorfer. 2010a. Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodiversity and Conservation 19:853-866. Parker P, E Buckles, H Farrington, K Petren, N Whiteman, R Ricklefs, J Bollmer & G Jiménez-Uzcátegui. 2011. 110 years of Avipoxvirus in the Galapagos Islands. PLoS ONE 6:e1 5989. Parker P & S Deem. 2012. Wildlife health monitoring and disease management. Protecting the biodiversity of Galapagos. En The role of Science for conservation. Pp. 165-177. Routledge, London. Parker P, N Whiteman & R Miller. 2006. Conservation medicine on the Galapagos Islands: partnerships among behavioral, population and veterinary scientists. The Auk 123:625-638. Petren K, P Grant, B Grant, A Clack & N Lescano. 2010. Multilocus genotypes from Charles Darwin’s finches: biodiversity lost desde the voyage of the Beagle. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365:1009-1018. Phillips R, D Wiedenfeld & H Snell. 2012. Current status of alien vertebrates in the Galapagos Islands: invasion history, distribution, and potential impacts. Biological Invasions 14:461-480. Steadman D. 1986. Holocene vertebrate fossils from Isla Floreana Galapagos Ecuador. Smithsonian Contributions to Zoology I-IV; 1-104. Steadman D. 2006. Extinction and biogeography of tropical Pacific birds. University of Chicago Press, Chicago. Swarth H. 1931. The avifauna of the Galapagos Islands. Occasional papers of the California Academy of Sciences 18:1-299. Sulloway, F. 1982. The Beagle collections of Darwin’s finches (Geospizinae). Bulletin of the British Museum of Natural History - Zoology Series 43: 48-94.

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Van Riper C, S van Riper, M Goff & M Laird. 1986. The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56:327-344. Watson J, M Trueman, M Tufet, S Henderson & R Atkinson. 2010. Mapping terrestrial anthropogenic degradation on the inhabited islands of the Galapagos archipelago. Oryx 44:79-82. Wiedenfeld D. 2006. Aves, The Galapagos Islands, Ecuador. Checklist 2:1-27. Wiedenfeld D, G Jiménez Uzcátegi, B Fessl, S Kleindorfer & J Valarezo. 2007. Distribution of the introduced parasitic fly Philornis downsi (Diptera, Muscidae) in the Galapagos Islands. Pacific Conservation Biology 13:14-19. Wiedenfeld D & G Jiménez Uzcátegui. 2008. Critical problems for bird conservation in the Galapagos Islands. Cotinga 29:22- 27. Wikelski M, J Foufopoulos, H Vargas & H Snell. 2004. Galapagos birds and disease: Invasive pathogens as threats for island species. Ecology and Society 9:5. [en línea] URL: http://www.ecologyandsociety.org/vol9/iss1/art5

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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

Photo: © Francesca Cunninghame ¹Charles Darwin Foundation ²Galapagos National Park Directorate ³Durrell Wildlife Conservation Trust ⁴San Diego Zoo Global

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 was deemed unfeasible (Fessl et al., 2010b). Consequently, not been evident until rat control measures were in mangrove finch conservation management maintained place (Cunninghame et al., 2015). This highlighted the an in situ focus with the aim of protecting and increasing importance of thorough field research and resulted in the wild population (Fessl et al., 2010b). additional management methodologies. Introduced rat control: 2007 to the present A stakeholder workshop in 2015 assessed past and present conservation management of the species, Introduced rat control at PTN and CB was initiated in 2007, resulting in the development of the 2016-2020 Mangrove with the installation of over 200 enclosed bait stations Finch Conservation Action Plan. This plan incorporates containing wax cube Klerat baits (0.01 parts per million all past research and management to ensure the most brodifacoum per kg). These are laid out in a 50-m grid effective conservation management for the species over throughout and around the periphery of the mangrove the next five years. Management of the species is both forests (Fessl et al., 2010b), and checked regularly and re- time intensive and expensive. Due to the precarious baited as necessary. Monitoring of introduced rats has situation of the mangrove finch, it is vital to ensure that revealed a reduction in rat numbers, while mangrove all techniques used result in the successful conservation finch nesting success showed an increase from 18 to 37 of the species. percent (Fessl et al., 2010a). In recent years, mangrove finch nest predation by rats has been relatively low, This article describes past and current management representing just 13% of failed nests (Figure 1). actions, provides an evaluation of results in relation to the long-term goals, and presents the next steps in the Due to continual reinvasion by rats into the mangroves, process. baiting must be constant to ensure that rat numbers are maintained at a low level and nest predation is low. Captive assurance population: 2007-2009 Current rat control methods are successful in maintaining rats at a low density; however, the long-term regular use Due to the extremely small population size of the of brodifacoum is against best practice policy according mangrove finch, the feasibility of a captive assurance to other countries due to the buildup of brodifacoum in population was assessed (Fessl et al., 2010b). A trial with the environment (Brown et al., 2015). Footprint tracking the more common, closely related woodpecker finch was (ink tunnel monitoring) of bait station consumption in conducted using specially built infrastructure in Puerto 2010-2011 revealed that even when rat numbers are low, Ayora (Fessl et al., 2010a; Good et al., 2009). Ten individuals invertebrates consume up to 30 g of bait per night per bait were held for up to 18 months, and although all birds station. Consequently, the amount of bait deployed has survived and were released into the wild following the been significantly reduced and rat monitoring intensified trial, due to logistical complications and disease risk, the from twice to four times a year. The current action plan establishment of a captive mangrove finch population proposes an adoption of more reactive control methods

70 2014 60 2015 50 2016 40

30

20

10

0 Failure: Failure: Failure: Failure: Success Nestling mortality Abandoned Predation Undetermined P. downsi eggs cause

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.

162 GALAPAGOS REPORT 2015 - 2016 to further reduce the amount of bait used, by monitoring Philornis downsi control: 2012 to the present with chew cards over larger areas and focusing control only in the areas where rats are detected. Moreover, self- Field research from 2010–2014 highlighted the impact of resetting, multi-kill traps (Goodnature New Zealand) could P. downsi parasitism on mangrove finch nestling survival be trialed on a small scale as a low maintenance non-toxic (Young et al., 2013; Cunninghame et al., 2015). Since control method (Carter et al., 2016). Additionally, plans 2011, this has been the principal cause for nest failure are underway to change to a less cumulative toxin, in (Cunninghame et al., 2015) (Figure 1). In collaboration conjunction with Island Conservation (IC) and the GNPD. with the Philornis Project (CDF/DPNG), trapping trials have been conducted in mangrove finch habitat and the Translocation: 2010 surrounding lava field since 2013 (Figure 2).

Expanding the range of the mangrove finch to reduce the Trapping at PTN, although using the same lures deployed risk of extinction by establishing additional populations with relative success on Santa Cruz, has not shown any within the historic range on Isabela is a priority (Fessl et evidence of success even in localized protection for al., 2010b; Cunninghame et al., 2011), especially since individual nests. There is still no viable method to protect the disappearance of the remnant population from mangrove finch nestlings in situ, which is a desired southeastern Isabela in 2009 (Cunninghame et al., 2013). outcome for the conservation of the species (Causton et A trial translocation moving nine birds from PTN to Bahia al., 2013). Current research into treating nests of other Urbina was conducted in 2010 (Cunninghame et al., 2011; passerine species on Santa Cruz could potentially offer a Cunninghame et al., 2013; Young et al., 2013). Long-term viable method for protecting mangrove finch nestlings establishment did not occur and four of the nine individuals in situ. have since been observed at the source population (Cunninghame et al., 2013). Although the reestablishment Head-starting: 2014 to the present of mangrove finches within their historic range continues to be a priority, the further translocation of juveniles or In order to increase the number of fledglings produced adults from PTN and/or CB has been suspended due to each season, head-starting of early laid mangrove finch the lack of a sizeable source population from which to clutches has taken place for three consecutive years take individuals (Cunninghame et al., 2015). Any future in collaboration with San Diego Zoo Global (SDZG) attempts to establish individuals in other areas should be (Cunninghame et al., 2015). Artificial egg incubation done using juveniles reared in captivity from eggs that and hand-rearing of nestlings in captivity, away from have a lower probability of survival in the wild. Moreover, the presence of P. downsi parasitism, has enabled 36 juveniles of certain species fledged at a new location are mangrove finch fledglings to be released over the past less likely to return to their natal site (Powesland et al., three seasons (Figure 3). 2013).

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

163 GALAPAGOS REPORT 2015 - 2016

16

14

12 Number captive-reared juveniles released 10 Number wild- edged 8 juveniles

6

4

2 0 2014 2015 2016

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.

Overall head-starting has been a success, especially when of released juveniles, following a soft release, has shown compared to the relatively small number (fewer than 20) 97% survival during the 21-day period while transmitter of wild fledglings produced (Figure 3). However, logistical batteries lasted. Nonetheless, the long-term impact challenges (delayed transport time of eggs from the of head-starting to increase population size remains field to captive-rearing facility) and complications with unknown. After radio-tracking ends, captive-reared equipment and captive-husbandry in 2015 highlighted mangrove finches can only be identified by observing the importance of establishing best practice protocols for the unique color band combinations on their right leg captive-rearing. Initial short-term telemetry monitoring (Figure 4).

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

Life history traits of the species, especially their cryptic data suggest that young birds use habitat outside of the behavior when not breeding, make monitoring of mangroves (Figures 5 & 6); whether juvenile birds spend non-breeding individuals unreliable (Fessl et al., 2011; long periods in the arid zone is unknown. Cunninghame et al., 2015). Moreover, initial dispersal

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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 next two years, any observations of juveniles released technique, captive-reared birds must be recruited into in 2014-2015 establishing territories or breeding will the breeding population (Snyder et al., 1996). For the indicate success of head-starting juveniles. mangrove finch, recruitment of juvenile birds into the breeding population appears to take several years during Head-starting is planned for four consecutive seasons which time it is difficult to obtain reliable data regarding through 2017. A subsequent evaluation will determine its the survival of captive-reared individuals. To date three success as a tool for increasing the size of the mangrove captive-reared individuals (Figure 7) have been observed finch population. Whenever a method for in situ protection two and one year post release, one of which was calling of nestlings from P. downsi parasitism is deemed viable with the correct mangrove finch call. These observations and the population appears to be in recovery, head- demonstrate that captive-reared mangrove finches are starting should be discontinued. capable of longer-term survival in the wild. During the

165 GALAPAGOS REPORT 2015 - 2016

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 not recognised until later, resulted in two pure woodpecker finch eggs being collected for head-starting in 2014 and Collection of mangrove finch blood samples for genetic the juveniles released (Lawson et al., in prep) (Figure 8). analysis has been conducted with the wild population This example highlights the importance of information since 1999; additionally, all captive-reared juveniles are gained from genetic sampling and analysis; however, few sampled (Fessl et al., 2010b; Cunninghame et al., 2015; changes can be made to management techniques in the Lawson et al., in prep). Recent analysis (L. Lawson) shows field if un-observed copulations sire offspring. a reduction in genetic diversity of the current population when compared to samples collected in 1899 and 1906, Recommendations for conservation which represent the more widespread and populous management of the mangrove finch: 2016–2020 historic population. Since captive-rearing was initiated in 2014, it has been possible to conduct paternity studies to Conservation management of the mangrove finch is better understand the breeding ecology of the mangrove required in the near to mid-term to ensure that the finch. This has shown two incidences of extra pair population survives and expands (Fessl et al., 2010a; Fessl et copulations (where the female of a nesting pair copulates al., 2010b; Cunninghame et al., 2015). Conservation of the with another male but continues to nest with her original species should be focused on the wild population, with any mate) (Lawson et al., in prep). The extent to which genetics birds reared in captivity being released at the end of each can be used to help maximize conservation management breeding season as independent juveniles. A combination of the mangrove finch is to be determined. Ideally, if head- of complementary research and management is required starting is continued, to help reduce over-representation in order to ensure that the actions succeed in reaching of certain individuals within the population, eggs should the long-term goal of increasing the population and be collected from a diverse range of breeding pairs. range of the mangrove finch. The following management However, with fewer than 20 breeding pairs remaining recommendations for the upcoming five years are (Cunninghame et al., 2015), coupled with the even lower proposed: number of pairs with nests during the collection period, it is likely that in future years all available nests will be • Conduct seasonal monitoring of the mangrove finch collected regardless of whether offspring from the same population (point counts, territory mapping, and pair have been reared in the past. nesting-breeding success) to determine population dynamics, and identify any downward trends; To date, over the three seasons, mangrove finch fledglings from 16 different pairs have been released back into the • Conduct in situ introduced rat control to ensure that wild. At least four of these pairs later reared their own nest predation is maintained at a low percentage; offspring. An extra-pair copulation of an unbanded female adopt best practice techniques; woodpecker finch (who had paired with a known banded male mangrove finch) with a male woodpecker finch and • Collaborate with the Philornis Project, and conduct

166 GALAPAGOS REPORT 2015 - 2016

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 account new parameters not included in the 2009 nest treatment methods at PTN; analysis, most notably the impact of P. downsi parasitism and head-starting; • Conduct head-starting for a minimum of one more season (totaling four), rearing at least eight individuals • Maintain political and financial support to ensure that per season; active conservation management of the Critically Endangered species continues. • Publish mangrove finch head-starting protocols during 2016; Acknowledgements

• Continue to focus on building capacity within local The bi-institutional Mangrove Finch Project of the partners and collaborators to lessen reliance on Charles Darwin Foundation and the Galapagos National international assistance; Park Directorate in collaboration with San Diego Zoo Global and Durrell Wildlife Conservation Trust is currently • Conduct monitoring of mangrove finch habitat to funded by Galapagos Conservation Trust, Marguerite better determine long-term survival of captive-reared Griffith-Jones, GESS Charitable Trust, Decoroom Limited, individuals; The Leona M. and Harry B. Helmsley Charitable Trust, International Community Foundation, Swiss Friends of • Use the thorough habitat assessment information the Galapagos, Foundation Ensemble, the British Embassy (Dvorak et al., 2004) to select a potential reintroduction in Quito, and several individual donors. The challenging site for captive-reared individuals if no natural field work would not have been possible without the dispersal to other mangrove sites is confirmed prior continued outstanding commitment and motivation of to 2018-2019; local and international field assistants and volunteers.

• Continue to collect genetic samples and work with collaborators for analysis to better inform management decisions; • Repeat Population Viability Analysis taking into

References BirdLife 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

Photo: © Luis Ortiz-Catedral 1Massey University, New Zealand 2Galapagos National Park Directorate 3Durrell Wildlife Conservation Trust

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

Methods 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 We visited the islets of Champion and Gardner-by-Floreana an average depth of 13.8 cm (± 1.7 cm). Each nest (n=8) during the breeding season (between February and April) consisted of approximately 198 ± 56 twigs that are 3-29 in 2011 and 2013, on trips with durations of four to seven cm long, mainly of Gabrowskia boerhaaviaefolia, Croton consecutive days, to document the presence of active scouleri, and Cordia lutea. Other nest-building materials nests, the status of the nests, clutch size, the number of included radius and ulna bones of frigatebirds (Fregata chicks per nest, and the composition of breeding groups. major), Nazca booby (Sula grantii) feathers, skin of the Once the chicks left the nest, we confirmed the cessation Galapagos snake (Pseudalsophis biserialis), and gecko of reproductive activities, and recorded the physical (Phyllodactylus baurii) skin, as well as leaves of Scalesia characteristics of the nests and the presence or absence of affinis. Clutch size ranged from one to four eggs (average P. downsi in the nest material. We also recorded the height 2.5 eggs), with egg dimensions of 26.0 x 18.4 mm (n=2). of the nest and the plant species on which it was built. Eggs were pale blue in color, with irregular brown spots Approximately three weeks after hatching, the chicks were (Figure 1). banded, using a unique combination of metal rings for each bird to allow individual identification. Each chick was Nest success and parasitism by Philornis downsi inspected for damage in their nostrils caused by P. downsi (see Causton et al., 2013). Incubation lasts 15 to 17 days and chicks leave the nest 13 to 16 days after hatching. They tend to remain in the To estimate population size on both islets, we carried out low vegetation a few centimeters from the base of the surveys using the mark:recapture methodology described plant where the nest is located. Of the 45 registered by Hoeck et al. (2010). The sampling area was equivalent nests, the emergence and development of chicks was to 20% of the total area of the current distribution of only observed for 17 nests, which produced an average the Floreana mockingbird, and therefore the global of 2.4 chicks (range 1-4 chicks). The rest of the observed population estimate is an extrapolation from the sampling nests failed due to egg predation (n=8), chick predation area estimates. (n=5), abandonment (n=3), or unknown causes (n=12). Pupae of P. downsi were found in only five nests (11%) Results and never more than 25 pupae were detected. A total of 101 chicks and juveniles were banded; none of them Nest characteristics had deformations in the nostrils or beak attributable to parasitism by P. downsi. 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 Deformations due to P. downsi were not observed in the m (range 0.4 m to 4 m). The nests were built in four species 170 adult birds banded during the same period. Although of native plants: Croton scouleri (n=22), Cordia lutea circumstantial, these observations and the low incidence (n=10), Gabrowskia boerhaaviaefolia (n=7), and Opuntia of nests with pupae of P. downsi indicate that this parasite megasperma (n=6). occurs at lower levels in this species than in other species of Galapagos birds, including the Galapagos mockingbird

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(Mimus parvulus) (Knutie et al., 2016; O’Connor et al., Population estimate 2010). It is not known which species prey on Floreana mockingbird eggs and chicks on Champion and Gardner- The estimate of the global population of Floreana by-Floreana, but we have observed Floreana mockingbirds mockingbirds has ranged from a maximum of 696 attacking groups of anis (Crotophaga ani) next to active individuals in November 2010, to a minimum of 435 nests. This species feeds on chicks of other birds (Connett individuals in June 2011. On average, the annual et al., 2013). We have also seen Floreana mockingbirds population size (2010-2012) is estimated at 578 attacking Galapagos snakes (Pseudalsophis biserialis), a individuals for the two islands (Figure 2). This population species that we have observed inspecting active finch size is greater than that estimated between 2003 and nests on Champion and Galapagos mockingbird nests on 2007 (i.e., 85-231 individuals), using transect counts Santa Cruz Island. (Jimenez-Uzcategui et al., 2011).

700

550

400

250 Number of mockingbirds

100 11-2010 12-2010 01-2011 03-2011 06-2011 08-2011 10-2011 12-2011 01-2012 03-2012 05-2012 Month - Year

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

Conclusions and recommendations megasperma in the lowlands of Floreana does not pose a limiting factor for the reintroduction of mockingbirds, Floreana mockingbirds, unlike several finch species and because other species such as Croton scouleri, Cordia lutea, Galapagos mockingbirds, appear to be less affected and Gabrowskia boerhaaviaefolia are common. Finally, by P. downsi, as indicated by the low frequency of this our population estimates suggest that the inter-annual parasite in the nests observed during this study, and variability in population size is less drastic than previously the non-existent evidence of deformation of nostrils in estimated (see Jimenez-Uzcategui et al., 2011). juveniles and adults. Our observations are consistent with the theory of that the acute intensity of parasitism In general terms, the next steps for the conservation of of P. downsi is associated with higher, humid areas in the species include: Galapagos (Wiedenfeld et al., 2007). 1. Development of an updated reintroduction plan with In planning a future reintroduction of the Floreana specific objectives and a general schedule of actions mockingbird to the island that it is named for, it would and their evaluation. be important to ascertain that the potential release sites exhibit low levels of parasitism of P. downsi. This can be 2. Development of a socialization plan with the verified by means of a study of finch species that inhabit community of Puerto Velasco Ibarra to identify local the lowlands of the island, as a precautionary measure attitudes towards the reintroduction of an endemic to minimize any impact of this parasite in the future species. development of mockingbird chicks. 3. Identification of potential reintroduction sites in the In general terms, the nesting of the Floreana mockingbird lowlands of Floreana, taking into account availability is similar to that of other mockingbird species in of food resources, structure of the habitat, and relative Galapagos. As suggested by Curry (1986), Floreana abundance of P. downsi. mockingbirds are not dependent on Opuntia megasperma for building nests. Therefore, the absence of Opuntia 4. Continuation of annual counts of the populations of

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Champion and Gardner-by-Floreana Islets to better Walter Chimborazo, Christian Pilamunga, Alonso Carrión, understand the population dynamics of this species. Fidelino Gaona, and to all the volunteers who helped in the field. We also thank Massey University, Durrell 5. Continuation of training staff, volunteers, and Wildlife Conservation Trust, Friends of Galapagos New Ecuadorian biologists. Zealand, Mohamed bin Zayed Species Conservation Fund, Galapagos Conservation Trust, and Galapagos Acknowledgments Conservancy Canada for financial support. The Charles Darwin Foundation provided valuable logistical assistance We would like to thank Estalin Jiménez, José Naula, and the University of Zurich provided field teams to Alizón Llerena, Milton Chugcho, Johannes Ramirez, complete multiple trips to the study sites.

References Causton 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

Photo: © James Gibbs 1Galapagos Conservancy 2State University of New York – College of Environmental Science and Forestry 3Galapagos National Park Directorate 4Yale University – Department of Ecology and Evolutionary Biology

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

A new era for giant tortoise restoration (Rueda and Carrión). Dr. Gisella Caccone leads the tortoise genetics team from her base at Yale University and In July 2012, an international workshop, Giant Tortoise provides critical guidance. The GTRI expands on decades Recovery through Integrated Research and Management, of tortoise research and management investments, and is was held in Galapagos. Building on the accomplishments currently focused on the following priority projects. of the last half-century of tortoise conservation, the workshop generated strategic and operational plans GTRI priorities for the next five years to guide the next few decades of tortoise research and management. Periodic review of the giant tortoise breeding and rearing centers. In November 2014, the first comprehensive review These plans coalesced into the GTRI, initiated in 2014, as of the three Galapagos National Park tortoise breeding and a collaborative effort of Galapagos Conservancy (GC), the rearing centers was carried out by a team that included GNPD, and a group of international scientists. The GTRI’s tortoise experts, a veterinarian with expertise in Galapagos primary goal is to re-align and expand conservation efforts tortoises, and Galapagos National Park personnel. The toward fully restoring the tortoise complex in numbers, team carried out visits to each center to review tortoise range, ecological impact, and economic importance health, condition of tortoise corrals, infrastructure and throughout the Archipelago. equipment, maintenance, and personnel. The goal of the periodic review is to ensure that improved and consistent To advance the GTRI, the GNPD provides technical protocols are used at all centers. Salary support for a critical and field expertise, logistical support, field personnel, staff position has also been provided. Out-of-country infrastructure, and the authorization to carry out the work. professional “re-tooling” opportunities overseas are being GC provides overall coordination and leadership, scientific funded and planned for selected center staff. Current plans advice, and strategic funding; ultimately GC plans to are underway to renovate the technology for incubating invest more than $1,000,000 in tortoise restoration. The tortoise eggs. Genetic analyses are currently being used small team that oversees the GTRI and coordinates its to improve breeding programs, beginning with tortoises suite of ambitious activities includes the Galapagos-based from Española and Pinzón. director of the Initiative (Tapia); the California, USA-based coordinator (Cayot); the New York, USA-based science Given that tortoise health issues, particularly of tortoises advisor (Gibbs); and Galapagos National Park technicians maintained in captivity, are of increasing concern, we have

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Figure 2. Park rangers releasing juvenile giant tortoises from the Española Island lineage to Santa Fe Island in June 2015. Photo: GNPD begun to compile and analyze the available information how tortoises repopulate an island and their future effects to identify problems and highlight knowledge gaps. In on the ecosystem. Notably, Santa Fe also now holds an collaboration with personnel of the University of Armed insurance colony of Española tortoises, listed as critically Forces of Ecuador (ESPE – Spanish acronym), we are endangered by the IUCN. carrying out laboratory tests to develop protocols for parasite and disease detection in tortoise blood and scats. Reestablishing giant tortoise populations on Pinta and Floreana Islands. One of the long-term goals of the GTRI is Return of giant tortoises to Santa Fe Island. Tortoises the reestablishment of reproductive tortoise populations once lived on Santa Fe Island in the central part of the on Floreana and Pinta Islands, where tortoises are now Archipelago but, sadly, the species has been extinct for extinct. In addition to reestablishing historical tortoise more than 150 years. To address the situation, the GTRI populations, doing so will contribute to restoration of the conducted a careful review including the definitiveness islands’ ecosystems. Repopulation of these islands is being of evidence of the former existence of an endemic Santa accomplished by recovering tortoises with significant Fe tortoise, potential positive and negative impacts of levels of their genomes showing ancestry from either tortoise restoration to the island’s ecosystem, possible Floreana or Pinta from Wolf Volcano on Isabela Island. Wolf sources of “analog” tortoises to replace the long-lost Volcano hosts an eclectic set of tortoises: a major GNPD- endemic form, and an evaluation of restoration alternatives organized expedition in 2008 and subsequent genetic based in part on modeling future tortoise reintroduction analysis of the blood samples collected (Garrick et al., 2012; scenarios (Tapia et al., 2015a). On the basis of accumulated Edwards et al., 2013) confirmed that tortoises were likely scientific knowledge, the GNPD implemented a plan to translocated to Wolf Volcano from around the Archipelago restore tortoises to the island using the genetically and during the whaling era when large numbers of tortoises morphologically similar Española tortoise (Poulakakis et were not only killed but also moved around the islands. A al., 2011). In June 2015, 201 juvenile Española tortoises major expedition, involving a large group of park rangers were released in the interior of Santa Fe Island (Figure and collaborating scientists, a support helicopter, and a 2). Annual releases of 60-80 tortoises are planned over research vessel onsite throughout the expedition, was the next ten years. Monitoring of tortoises, endemic carried out in November 2015 (Figures 3-5). Thirty-two land iguanas, and vegetation is carried out regularly. A tortoises with shell features similar to the known Floreana 2016 resurvey confirmed that apparently all tortoises and/or Pinta hybrids were transferred to the Fausto released had survived their first year, far exceeding the Llerena Tortoise Center on Santa Cruz Island and blood 50% survival rate expected. The island is relatively pristine samples were taken from over 180 other tortoises with and monitoring data will provide vital information about similar features that remain on the volcano. Detailed plans

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for breeding programs are being developed to produce on Pinta Island in 2010 after a lifetime in captivity, gaining young tortoises to repopulate Floreana and Pinta Islands. an average of 10 kg in the first year (Hunter, 2013). As on Some tortoises, properly quarantined, may be transferred Santa Fe, monitoring programs will track the tortoises directly from Wolf Volcano to Floreana or Pinta. Tortoises through the years following release on their new home in this program are expected to thrive when released on islands. their home islands, as did the sterilized tortoises released

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 has, however, never been an expedition to systematically ecological engineers, and improving tortoise habitat. search for the tortoises of Fernandina. The GTRI is working Re-conceptualizing giant tortoises not just as fascinating to catalyze a search across the island, using a combination biological creatures but as agents of ecosystem dynamics, of newly available high resolution satellite imagery, low‐ that is, as ecosystem engineers (Gibbs et al., 2009), has level helicopter surveying, ground‐level exploration of expanded the rationale for tortoise restoration. Tortoise the most promising tortoise hotspots identified from the restoration is not just about tortoises; it’s also about air, and exploration of caves likely to contain remains of ecosystem restoration and, more generally, advancing tortoises. island restoration in Galapagos. However, we do not yet fully understand how tortoises shape the ecosystems and Genetic data are similarly puzzling. Mitochondrial DNA biological communities in which they live. To this end, an data suggest that the one individual collected shares elaborate system of tortoise “exclosures” centered around a similar haplotype with tortoises from C. porteri from cactus, along with companion “control” plots, has been Santa Cruz, a haplotype that has never been found in established on both Española and Santa Fe Islands (Figure the geographically closer southern and central Isabela 6). Annual monitoring is beginning to reveal the impact species. This could suggest a recent human-mediated of tortoises on plant communities, especially cactus, in movement. However, given that the same haplotype has ways both positive (facilitating sexual reproduction via not been recovered in the extant population of C. porteri seed dispersal) and negative (eating pads and reducing and that C. porteri is not saddleback as is the Fernandina asexual reproduction). A large-scale, archipelago- specimen, it could be that Fernandina was colonized long wide status survey of Opuntia, with emphasis on the ago by an ancestor of the same lineage that gave rise to C. lower, arid islands, is anticipated in the years ahead porteri. In this second scenario, either through vicariance to better understand the status of these plants vital to or dispersal through the Perry Isthmus, a few domed the expansion of tortoise populations throughout the tortoises arrived on Fernandina and evolved into a new Archipelago. saddleback species. Ongoing genome-wide analyses will permit a test of these two hypotheses. Population surveys and advanced genetic sampling in San Cristóbal, Pinzón, southern Isabela, Santiago, and Evaluation and mitigation of human interactions with other islands. During the tortoise workshop in 2012, and impact on giant tortoises. Giant tortoises were a several knowledge gaps were identified, including the traditional part of the diet of settlers in Galapagos. When general lack of knowledge of the status of some extant the Galapagos National Park was established in 1959, populations, such as the Cerro Fatal tortoises, those efforts to curb the hunting of tortoises were generally of Wolf and Darwin Volcanos, and the San Cristóbal successful. However, killing tortoises underwent a population. These will be the focus of intensive population resurgence on Isabela Island in the 1990s (Cayot & Lewis, surveys in the next few years. We also need additional 1994) and has become a serious concern on southern knowledge of the genetic relationships and evolutionary Isabela, where the largest tortoise populations in the distinctiveness of tortoises from different areas. In some entire Archipelago once occurred, particularly on Sierra cases, tortoise populations now considered one species Negra. There, the human-tortoise conflicts need to be should probably be classified as two or more distinct resolved. On Santa Cruz and San Cristóbal Islands there species. An example of a recently identified species, are increased road systems and infrastructure in the based on results of genetic analysis, is the eastern Santa highlands that could be altering tortoise movements. Cruz Island tortoise (Chelinoidis donfaustoi) from the An expanded program involving GTRI, along with the Cerro Fatal area, named in honor of the distinguished Galapagos Biosecurity Agency and the Charles Darwin park ranger and tortoise caretaker Don Fausto Llerena Foundation, will generate guidelines to mitigate any (Poulakakis et al. 2015; Figure 7). GTRI seeks to facilitate identified problems; actions will potentially include collaborations between outside scientists and GNPD to education, community outreach, establishing migration combine modern genetic analysis with boots-on-the- corridors, adapting best management practices for ground surveys to help resolve the many unknowns habitat, and enforcement. about various tortoise populations, thereby fostering more effective conservation. Lonesome George. Coincidentally the death of Lonesome George occurred on the eve of the convening of the Fernandina exploration. Since 1906, with the collection international giant tortoise workshop in 2012. Amongst of a single specimen on Fernandina by the California the tears and choked voices of workshop participants Academy of Sciences, there has been evidence that emerged a strong sentiment to realize the words inscribed a mysterious species of giant tortoise—Chelonoidis on the information panel adjacent to Lonesome George’s phantastica—or fantastic giant tortoise might exist old enclosure at the Fausto Llerena Tortoise Center: somewhere on the island. Since the specimen collected “Whatever happens to this single animal, let him always in 1906, there have been three independent observations remind us that the fate of all living things on Earth is in (primarily tortoise scat) suggesting that a few tortoises human hands.” Lonesome George’s death inspired the may still remain on the largely unexplored island. There workshop participants to “think big” and expand the

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

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 international team including: the laboratories of Kevin very pragmatic terms, the GTRI has invested tremendous White at the University of Chicago (USA), Carlos Lopez- resources in preserving the conservation legacy of Otin at the University of Oviedo (Spain), and the Caccone Lonesome George for the people of Ecuador and the team at Yale. This work is paralleled by development of larger world by orchestrating his temporary re-location to genome-wide markers (SNPs, Single Copy Polymorphic the New York City area to be taxidermied by world-class markers) to study the neutral and adaptive component of experts for return to Galapagos where the tortoise will be the Galapagos tortoise genome. This will provide insights ensconced in the newly renovated tortoise rearing center on morphological and life history traits that make these visitation site (Figure 8). There he will continue to remind animals unique, facilitate the identification of individuals us of the constant need to work together to prevent future of high conservation value for restoring threatened or extinctions of all species. A beloved family member will extinct tortoise populations, and help to understand the also be able to rest back home again. relative importance of environmental features in shaping the existing genetic variability, which in turn will help to Prior to the workshop in 2012, an effort to sequence understand potential impacts of climate change on these the entire genome of Lonesome George had begun. animals. This collaborative effort is ongoing and involves an

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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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Conclusion and next steps Please follow the GTRI blog at Galapagos Conservancy’s website for the latest news about this evolving, The GTRI takes as its role model the first tortoises released collaborative effort to fully restore these magnificent to Española in 1971 by the GNPD and the CDRS; those creatures. tortoises initiated the recovery of a species that at one time was on the verge of extinction but now has a Acknowledgments burgeoning population of more than 1000 tortoises thriving and reproducing on the island (Gibbs et al., 2014). We would like to thank all of those who have worked for In a similar slow, tortoise-like fashion, we hope that the tortoise conservation over the last half century, all of those programs we are launching during these first five years of who participated in the tortoise workshop in 2012, and all the GTRI will provide the necessary seeds for an extended of the park rangers, volunteers, and scientists who continue program of self-restoration and population growth by the to work with us to ensure that the GTRI is a success. We tortoises themselves throughout the Archipelago. We are would also like to thank Galapagos Conservancy members off to a good start thanks to the ideas generated at the who support these efforts, as well as the Phillips Family 2012 tortoise workshop, the hard work and dedication Foundation, Mohamed bin Zayed Species Conservation of the GNPD, the collaboration of international scientists, Fund, Fondation Ensemble, Lawrence Foundation, Oak and the spark that Lonesome George’s death produced Foundation, Turtle Conservancy, and other groups that to motivate us to strive even harder to restore the giant provide support for the international scientists who are tortoise populations of Galapagos. an integral part of the GTRI.

References Caccone 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.

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Total number and current status of species introduced and intercepted in the Galapagos Islands

Charlotte E. Causton1, Heinke Jäger1, María Verónica Toral Granda2, Marilyn Cruz3, Manuel Mejía3, Erika Guerrero3 and Christian Sevilla4

Photo: © Heinke Jäger 1Charles Darwin Foundation 2Charles Darwin University, Darwin, Australia 3Galapagos Biosecurity Agency (ABG) 4Galapagos National Park Directorate 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 3. Some groups of organisms have not been surveyed transport vehicles or cargo during biosecurity inspections. adequately, for example Hymenoptera (e.g., These species are not established in Galapagos. Monitoring microwasps) and soil organisms. of transport vehicles allows the timely detection of alien species entering Galapagos and reduces the risk of 4. There are specimens awaiting identification. establishment. 5. There are about 50 plant species whose status is There are 17 species that are from historical records currently unknown; they could either be native or only (species may not have established or reports were introduced (a pollen or sediment analysis is required erroneous). Four species have been eradicated under for confirmation); management programs: rock pigeon (Columba livia); tilapia (Oreochromis niloticus); kudzu (Pueraria phaseoloides), and 6. Data on interceptions made by inspectors of the an Opuntia species. The confirmation of the eradication of Galapagos Inspection and Quarantine System a blackberry species (Rubus megalococcus) is pending. (SICGAL – Spanish acronym), the organization responsible for quarantine prior to the establishment Regarding the means by which they arrived in the islands, in 2012 of the Galapagos Biosecurity Agency (ABG – 825 species (52%) arrived accidentally as contaminants Spanish acronym), have not been included. or stowaways, and 724 species (46%) were introduced intentionally. For 2% of the species, the introduction Recommendations pathway is unknown or questionable (Table 1). 1. Merge all introduced species data into a single Introduced species currently established in the database, which will enable: Galapagos a) A continuously updated checklist and updated There are 1476 introduced species that have been reported taxonomic collection in a single site, thus as established in Galapagos: 810 terrestrial plant species facilitating scientific research; (including varieties and cultivars); 499 insect species; 70 species of other terrestrial invertebrates; 63 pathogens; b) Introduced species list accessible to all users; 27 vertebrate species, including a fish found in coastal lagoons; five marine invertebrate species, and two marine c) Continuous contribution by institutions with plants. information on introduced species.

Of the species established in Galapagos, 868 (58.8%) are 2. Establish a protocol for all institutions regarding the naturalized with self-sustaining populations, with insects collection and processing of introduced species data (467) and terrestrial plants (270) the main taxonomic and their introduction pathways to Galapagos. This groups (Table 1). Approximately 37.2% (549) are human- should have a standard format that facilitates the dependent or restricted to human settlements and there entry and subsequent use of this data. is no evidence of dispersal to areas of the Galapagos National Park. Of these, most are terrestrial plants (534). 3. Publish an annual report updating the number and Additionally, 2.3% of the species are possibly exclusively status of species introduced to the Galapagos Islands. associated with introduced species. The status of 1.7% of the species has not been determined (Table 1). Acknowledgements

Discussion This evaluation would not have been possible without the help of Leon Baert, Sharon Deem, Diana Flores, Anne The actual number of species introduced in Galapagos is Guézou, Brand Phillips, Víctor Carrión, Henri Herrera, likely to be higher than the number currently reported due Patricia Jaramillo, Gustavo Jiménez, Inti Keith, Patricia to the following factors: Parker, Brad Sinclair, Alan Tye, Mónica Ramos, Marcelo Montesdeoca, Nancy Duran, Alex Fonseca, Marco 1. Not all the results from taxonomic and species reviews Echeverría, Duglas Acuria, Rafael Conde, Rommel Iturbide, published in the last five years have been entered into Ronal Azuero, Viviana Duque, Alberto Vélez and other CDF’s Datazone. This is especially true for new reports technicians at ABG. We also thank GNPD for their continual of introduced insects and microorganisms. support.

2. Preliminary results from marine habitat censuses suggest that there are more introduced species than currently reported.

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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 Total Insects Marine Terrestrial Pathogens Vertebrates invertebrates invertebrates Marine plants Terrestrial plants Terrestrial

Naturalized 5 2 38 467 68 270 18 868 Human dependent 7 534 8 549 Coexists with introduced Established 17 15 2 34 species Present but status not 8 10 6 1 25 determined

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

Eradicated 2 2 4 Absent Historical record 1 8 8 17 Intercepted 15 38 7 9 13 82 Total number of introduced and intercepted 21 2 63 545 77 821 50 1579 species (including absent species)

Introduction pathway Total Insects Marine Terrestrial Pathogens Vertebrates invertebrates invertebrates Marine plants Terrestrial plants Terrestrial

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 21 2 63 545 77 821 50 1579 species (including absent species)

References Atkinson R, MR Gardener, G Harper & V Carrion. 2012. Fifty years of eradication as a conservation tool in Galápagos: what are the limits? Pp. 183–198. En: M Wolff & MR Gardener (eds.). The Role of Science for Conservation. Routledge, Oxon, UK.

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.

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