Macaronesia as a Fruitful Arena for Ecology, Evolution, and Conservation Biology

Abstract

Research in Macaronesia has led to substantial advances in ecology, evolution and conservation biology. We review the scientific developments achieved in this region, and outline promising research avenues enhancing conservation. Some of these discoveries indicate that the Macaronesian flora and fauna are composed of rather young lineages, not Tertiary relicts, predominantly of European origin. Macaronesia also seems to be an important source region for back-colonisation of continental fringe regions on both sides of the Atlantic. This group of archipelagos (Azores, Madeira, Selvagens, Canary Islands, and Cabo Verde) has been crucial to learn about the particularities of macroecological patterns and interaction networks on islands, providing evidence for the development of the General Dynamic Model of oceanic island biogeography and subsequent updates. However, in addition to exceptionally high richness of endemic species, Macaronesia is also home to a growing number of threatened species, along with invasive alien plants and animals. Several innovative conservation and management actions are in place to protect its biodiversity from these and other drivers of global change. The Macaronesian Islands are a well-suited field of study for island ecology and evolution research, mostly due to its special geological layout with 40 islands grouped within five archipelagos differing in geological age, climate and isolation. A large amount of data is now available for several groups of organisms on and around many of these islands. However, continued efforts should be made toward compiling new information on their biodiversity, to pursue various fruitful research avenues and develop appropriate conservation management tools.

Full text

fevo-09-718169 November 1, 2021 Time: 13:44 # 1
REVIEW
published: 05 November 2021
doi: 10.3389/fevo.2021.718169
Edited by:
Domingos Cardoso,
Federal University of Bahia, Brazil
Reviewed by:
Nuria Macías Hernandez,
University of La Laguna, Spain
Qin Li,
Field Museum of Natural History,
United States
*Correspondence:
Margarita Florencio
margarita.florencio@uam.es;
mflorenciodiaz@gmail.com
†Deceased
Specialty section:
This article was submitted to
Biogeography and Macroecology,
a section of the journal
Frontiers in Ecology and Evolution
Received: 31 May 2021
Accepted: 04 October 2021
Published: 05 November 2021
Citation:
Florencio M, Patiño J, Nogué S,
Traveset A, Borges PAV, Schaefer H,
Amorim IR, Arnedo M, Ávila SP,
Cardoso P, de Nascimento L,
Fernández-Palacios JM, Gabriel SI,
Gil A, Gonçalves V, Haroun R,
Illera JC, López-Darias M, Martínez A,
Martins GM, Neto AI, Nogales M,
Oromí P, Rando JC, Raposeiro PM,
Rigal F, Romeiras MM, Silva L,
Valido A, Vanderpoorten A,
Vasconcelos R and Santos AMC
(2021) Macaronesia as a Fruitful
Arena for Ecology, Evolution,
and Conservation Biology.
Front. Ecol. Evol. 9:718169.
doi: 10.3389/fevo.2021.718169
Macaronesia as a Fruitful Arena for
Ecology, Evolution, and Conservation
Biology
Margarita Florencio1,2,3,4,5*, Jairo Patiño3,6,7 , Sandra Nogué8, Anna Traveset9,
Paulo A. V. Borges3, Hanno Schaefer10, Isabel R. Amorim3, Miquel Arnedo11,
Sérgio P. Ávila12,13, Pedro Cardoso3,14, Lea de Nascimento15,16,
José María Fernández-Palacios15 , Sofia I. Gabriel17,18, Artur Gil3,19, Vítor Gonçalves12,13,
Ricardo Haroun20 , Juan Carlos Illera21, Marta López-Darias7, Alejandro Martínez22 ,
Gustavo M. Martins12 , Ana I. Neto3,13†, Manuel Nogales7, Pedro Oromí23,
Juan Carlos Rando23 , Pedro M. Raposeiro12,13, François Rigal3,24, Maria M. Romeiras3,25,
Luís Silva12,13 , Alfredo Valido7, Alain Vanderpoorten3, Raquel Vasconcelos26,27 and
Ana M. C. Santos3,4,28,29
1Department of Life Sciences, Universidad de Alcalá, Alcala de Henares, Spain, 2Departamento de Ecologia, Universidade
Federal de Goiás, Câmpus Samambaia, Goiânia, Brazil, 3Azorean Biodiversity Group, cE3c – Centre for Ecology, Evolution
and Environmental Changes, Universidade dos Açores, Azores, Portugal, 4Centro de Investigación en Biodiversidad y
Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, Madrid, Spain, 5Inland-Water Ecosystems Team -I-WET,
Departamento de Ecología, Edificio de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, Madrid, Spain,
6Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de La Laguna, La Laguna, Tenerife, Spain, 7Island
Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), La Laguna, Tenerife,
Spain, 8School of Geography and Environmental Science, University of Southampton, Southampton, United Kingdom,
9Global Change Research Group, Institut Mediterrani d’Estudis Avançats (CSIC-UIB), Esporles, Mallorca, Spain, 10 Plant
Biodiversity Research, Department of Ecology and Ecosystem Management, Technical University of Munich, Freising,
Germany, 11 Department of Evolutionary Biology, Ecology and Environmental Sciences, Biodiversity Research Institute -
IRBio, Universitat de Barcelona, Barcelona, Spain, 12 InBIO Laboratório Associado, Pólo dos Açores, CIBIO, Centro
de Investigação em Biodiversidade e Recursos Genéticos, Ponta Delgada, Açores, Portugal, 13 Departamento de Biologia,
Faculdade de Ciências e Tecnologia, Universidade dos Açores, Ponta Delgada, Açores, Portugal, 14 Laboratory
for Integrative Biodiversity Research - LIBRe, Finnish Museum of Natural History, University of Helsinki, Helsinki, Finland,
15 Island Ecology and Biogeography Group, Instituto Universitario de Enfermedades Tropicales y Salud Pública de Canarias
(IUETSPC), Universidad de La Laguna (ULL), La Laguna, Tenerife, Spain, 16 Long-Term Ecology Laboratory, Manaaki
Whenua - Landcare Research, Lincoln, New Zealand, 17 Departamento de Biologia Animal, Faculdade de Ciências, CESAM -
Centro de Estudos do Ambiente e do Mar, Universidade de Lisboa, Lisbon, Portugal, 18 Departamento de Biologia,
Universidade de Aveiro, Aveiro, Portugal, 19 IVAR - Research Institute for Volcanology and Risks Assessment, University
of the Azores, Ponta Delgada, Azores, Portugal, 20 Biodiversity and Conservation, Research Institute ECOAQUA, University
of Las Palmas de Gran Canaria, Telde, Gran Canaria, Spain, 21 Biodiversity Research Institute (CSIC-Oviedo
University-Principality of Asturias), Oviedo University, Mieres, Spain, 22 Molecular Ecology Group - MEG, Water Research
Institute (IRSA), National Research Council of Italy (CNR), Verbania Pallanza, Italy, 23 Departamento de Biología Animal,
Edafología y Geología, Universidad de La Laguna, La Laguna, Tenerife, Spain, 24 CNRS - Universiteé de Pau et des Pays
de l’Adour – E2S UPPA, Institut des Sciences Analytiques et de Physico-Chimie pour l’Environnementet les Materiaux, Pau,
France, 25 Linking Landscape, Environment, Agriculture and Food - LEAF, Instituto Superior de Agronomia (ISA),
Universidade de Lisboa, Lisbon, Portugal, 26 BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO,
Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto,
Vairão, Portugal, 27 Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain, 28 Global Change
Ecology and Evolution Group - GLOCEE, Department of Life Sciences, Universidad de Alcalá, Alcalá de Henares, Spain,
29 Terrestrial Ecology Group (TEG-UAM), Departamento de Ecología, Universidad Autónoma de Madrid, Madrid, Spain
Research in Macaronesia has led to substantial advances in ecology, evolution and
conservation biology. We review the scientific developments achieved in this region, and
outline promising research avenues enhancing conservation. Some of these discoveries
indicate that the Macaronesian flora and fauna are composed of rather young lineages,
not Tertiary relicts, predominantly of European origin. Macaronesia also seems to be an
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Florencio et al. Macaronesia as a Research Hotspot
important source region for back-colonisation of continental fringe regions on both sides
of the Atlantic. This group of archipelagos (Azores, Madeira, Selvagens, Canary Islands,
and Cabo Verde) has been crucial to learn about the particularities of macroecological
patterns and interaction networks on islands, providing evidence for the development of
the General Dynamic Model of oceanic island biogeography and subsequent updates.
However, in addition to exceptionally high richness of endemic species, Macaronesia
is also home to a growing number of threatened species, along with invasive alien
plants and animals. Several innovative conservation and management actions are in
place to protect its biodiversity from these and other drivers of global change. The
Macaronesian Islands are a well-suited field of study for island ecology and evolution
research, mostly due to its special geological layout with 40 islands grouped within
five archipelagos differing in geological age, climate and isolation. A large amount of
data is now available for several groups of organisms on and around many of these
islands. However, continued efforts should be made toward compiling new information
on their biodiversity, to pursue various fruitful research avenues and develop appropriate
conservation management tools.
Keywords: alien species, biodiversity hotspot, biotic interactions, extinction, long distance dispersal, reverse
colonisation, speciation, volcanic oceanic islands
INTRODUCTION
Oceanic islands have long fascinated biologists, as they provide
insights that have been incorporated into a number of ecological
and evolutionary theories. Today, research on island systems is
in the spotlight, with exciting new developments (e.g., Santos
et al., 2016;Patiño et al., 2017;Whittaker et al., 2017;Valente
et al., 2020). Many of these advances stem from studies performed
partially or entirely in Macaronesia (sensu Engler, 1914), a region
located in the Northeast Atlantic Ocean formed by the volcanic
archipelagos of the Azores, Madeira, Selvagens, Canary Islands,
and Cabo Verde (Figure 1).
Macaronesia comprises 40 islands and islets larger than 1 km2,
covering a latitudinal range from 14.8◦N to 39.7◦N (Figure 1 and
Table 1) and extending over a distance of almost 3,000 km. This
encompasses a strong climatic gradient from oceanic temperate
climate in the Azores, to Mediterranean climate in Madeira,
the Selvagens and Canary Islands, and warm arid climate in
Cabo Verde (Fernández-Palacios, 2010). The geological age of
the extant (emerged) islands and islets ranges from less than
35,000 years for Alegranza in the Canary Islands, to 25.7 million
years (Ma) for Selvagem Grande. However, seamounts around
Madeira and the Canary Islands are as old as 67 Ma (Gettysburg
near Madeira), which indicates that Macaronesia is at least twice
or three times older than its oldest emerged land (Fernández-
Palacios et al., 2011;Ávila et al., 2016). Furthermore, these
islands show contrasting levels of geographical isolation from the
mainland, varying from 96 km off North Africa (Fuerteventura,
Canary Islands) to more than 1,500 km (Flores, Azores) off
the Iberian Peninsula (Fernández-Palacios, 2010;Figure 1). The
boundaries of Macaronesia in the marine realm differ slightly,
as Cabo Verde is described as pertaining to a different province,
and the rest of the archipelagos are included in the Lusitanian
province (Freitas et al., 2019).
The wide latitudinal, altitudinal, size, and climate variations
of the Macaronesian islands are in part responsible for the
diversity of habitats they host. These range from desert and
semi-arid vegetation, typical for most of Cabo Verde and
the driest areas of the Selvagens and Canary Islands, to the
humid laurel and juniper forests characteristic of the Azores,
Madeira, and the mid to high altitudes of the western and
central Canary Islands (del Arco-Aguilar et al., 2010;Fernández-
Palacios, 2010). In addition, there are unique lentic and lotic
ecosystems (Hughes and Malmqvist, 2005), as well as important
microhabitats like subterranean cavities and volcanic hot springs
(see Pipan et al., 2010). Macaronesia also straddles a wide range
of marine habitats, which support a rich and yet incompletely
known marine biota (Moro et al., 2003;Tuya and Haroun, 2009;
Cordeiro et al., 2015).
In general, endemism appears to be high in many taxonomic
groups, particularly from the terrestrial realm, like vascular
plants, land snails and arthropods (Figure 2A and ESM1 in
Supplementary Material). Indeed, a truly remarkable data is
the percentage of endemic terrestrial mollusc species, that
reaches over 41% in Azores (potentially close to 91% once the
colonisation status is assigned to all species; Frias Martins, A.,
pers. comm.) and Cabo Verde, over 84% in Madeira (Teixeira,
D., pers. comm.), and over 94% in the Canary Islands. Despite
its small area, the Selvagens host over 50 endemic species
(over the 15% of the total number of native species), sharing
other endemisms with different Macaronesian archipelagos
(Fernández-Palacios, 2010). In the Canary Islands, the level of
endemism reaches 66% in spiders (Cardoso et al., 2010), and
100% in reptiles (Loureiro et al., 2008;Arechavaleta et al., 2010;
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FIGURE 1 | Geographical location of the Macaronesian archipelagos, with indication of the number of islands and their geological age (only islets >1 km2were
included; see Table 1).
Vasconcelos et al., 2013); within this context, almost 50% of
the plant species of the Canary Islands are endemics (Reyes-
Betancort et al., 2008), with over 70% of them being considered
single-island endemics (Carine and Schaefer, 2010). Finally, this
pattern of high endemicity is not so evident in marine ecosystems
(Figure 2B and ESM1 in Supplementary Material), where for
many groups, the number of endemic species does not even
reach 6% of the archipelagic biodiversity (Freitas et al., 2019); the
gastropods constitute the exception to this trend, particularly in
Cabo Verde, where the number of endemic species represents
over 44% of all native species (e.g., 86 Conus species inhabit
this archipelago, being its majority endemic to Cabo Verde;
Freitas et al., 2019).
Even though our knowledge of the flora and fauna of
Macaronesia is still far from complete, the collective effort
of systematists, ecologists, and biogeographers has resulted
in the compilation of comprehensive data sets for species
distributions (e.g., Arechavaleta et al., 2005;Borges et al., 2008,
2010;Arechavaleta et al., 2010;Romeiras et al., 2016a;Freitas
et al., 2019), morphological traits (e.g., Schaefer et al., 2011;
Whittaker et al., 2014;Henriques et al., 2017;Rigal et al.,
2018;Macías-Hernández et al., 2020), ecological history and
phylogenetic relationships (e.g., Emerson, 2002;Carine et al.,
2010;Amorim et al., 2012;Caujapé-Castells et al., 2017), and
species interactions (e.g., Dupont and Skov, 2004;Valido et al.,
2004;Valido and Olesen, 2010;González-Castro et al., 2012).
Nevertheless, despite the long-standing interest in Macaronesian
biodiversity, our knowledge of the different archipelagos and
taxa is still unbalanced, and the existing literature is rather
heterogeneous (see Lobo and Borges, 2010;Romeiras et al., 2019).
For example, the study of Cabo Verde’s biota lags behind that of
other Macaronesian archipelagos (Romeiras et al., 2020), which
is probably associated with the fact that many endemic species
only occur in habitats that are difficult to access, such as cliffs
in the mountain areas (Neto et al., 2020). Certain taxonomic
groups, like Platyhelminthes, Nematoda and Annelida, as well as
the Bacillariophyta and Amoebozoa typical of freshwater habitats
(but see Ritter et al., 2020;Gonçalves et al., 2021 for Madeira),
are still poorly studied in most archipelagos (Figure 2A and
ESM1 in Supplementary Material). Even in the case of terrestrial
arthropods, a group that has been intensively studied in the last
decades, species description is far from complete, with estimates
indicating that a large number of species remains unknown
(Lobo and Borges, 2010).
Human activity has drastically transformed Macaronesia (e.g.,
Borges et al., 2019), leading to profound changes in habitat
diversity and community composition over a relatively short
period of time (del Arco-Aguilar et al., 2010;Triantis et al.,
2010;Illera et al., 2012;Boieiro et al., 2018). Although the
documented European colonisation of Macaronesia only started
about 600 years ago, increasing evidence points to much earlier
human arrivals in some of the archipelagos (see Förster et al.,
2009;Gabriel et al., 2015;Rull et al., 2017). However, it was
not until Europeans started to settle on the islands that intense
land transformation and introduction of alien species led to a
more sudden and profound alteration in most native terrestrial
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TABLE 1 | Main characteristics of the islands and islets larger than 1 km2included in the Macaronesian archipelagos of the Azores, Madeira, Selvagens, Canary Islands,
and Cabo Verde (compiled from Geldmacher et al., 2001;Torres et al., 2002;Madeira et al., 2005;Azevedo and Portugal Ferreira, 2006;Holm et al., 2006;Ancochea
et al., 2010;Dyhr and Holm, 2010;Madeira et al., 2010;Ramalho, 2011;Ancochea et al., 2012;van den Bogaard, 2013;Aranda et al., 2014;Johnson et al., 2014;
Ancochea et al., 2015;Costa et al., 2015;Ramalho et al., 2015;Ávila et al., 2016 and references therein; Ramalho et al., 2017;Samrock et al., 2018;Marques et al.,
2020;Cornu et al., 2021).
Archipelago/
Island
Latitude Longitude Area (km2) Distance from
continent (km)
Distance from
closest island
(km)
Geological age of the
oldest subaerial
lavas (Ma)
Maximum altitude
(m asl)
AZORES
Corvo 39.6991 −31.1052 17 1,858 18 1.5 718
Flores 39.4419 −31.2025 143 1,864 18 2.16 913
Graciosa 39.0523 −28.0113 62 1,596 36 0.7 398
Terceira 38.7239 −27.2123 400 1,520 37 0.4 1,020
São Jorge 38.6372 −28.0292 246 1,584 18 1.85 1,067
Faial 38.5782 −28.7013 173 1,657 6 0.85 1,043
Pico 38.4695 −28.3336 436 1,610 6 0.19 2,351
São Miguel 37.7954 −25.4819 750 1,368 80 0.79 1,103
Santa Maria 36.9713 −25.0998 97 1,376 80 6.01 587
MADEIRA
Porto Santo 33.0692 −16.3422 40 633 39 18.8 517
Ilhéu da Cal 33.0466 −16.3855 1.4 641 0.4 NA 178
Madeira 32.7463 −16.9991 740 639 24 7.0 1,850
Deserta Grande 32.5390 −16.5205 10 640 21 5.5 479
Bugio 32.4243 −16.4856 3 636 33.7 5.5 388
SELVAGENS
Selvagem Grande 30.1453 −15.8656 3 374 18 25.7 153
CANARY ISLANDS
Alegranza 29.4023 −13.5148 10 169 10 >0.035 289
Montaña Clara 29.2990 −13.5365 1 160 2 0.039 256
La Graciosa 29.2554 −13.5032 27.5 152 1 0.05 266
Lanzarote 29.0245 −13.6418 796 125 11 15.0 670
Lobos 28.7514 −13.8245 4 123 2 NA 122
La Palma 28.6899 −17.8583 729 414 57 1.7 2,425
Fuerteventura 28.4061 −14.0365 1,725 96 11 23.0 807
Tenerife 28.2911 −16.5563 2,058 286 28 12.0 3,718
La Gomera 28.1174 −17.2326 378 333 28 11.0 1,484
Gran Canaria 27.9548 −15.5932 1,532 195 61 15.0 1,950
El Hierro 27.7465 −18.0066 278 381 61 1.1 1,501
CABO VERDE
Santo Antão 17.0565 −25.1701 779 834 13 7.57 1,979
São Vicente 16.8455 −24.9678 227 818 8 6.1 725
Santa Luzia 16.7663 −24.7452 35 797 8 7.0 351
Sal 16.7372 −22.9314 216 650 39 15.8 406
Branco 16.6543 −24.6682 2.8 792 7.6 6.0 327
Raso 16.6166 −24.5861 5.8 783 15.4 2.30 164
São Nicolau 16.5985 −24.2562 343 721 30 3.7 1,304
Boavista 16.0983 −22.8139 620 611 39 16.4–17.5 390
Maio 15.2180 −23.1606 269 614 26 11.9 436
Santiago 15.0837 −23.6248 991 634 26 2.39–2.87 1,392
Ilhéu de Cima 14.9731 −24.6330 1.5 772 8.2 NA 77
Ilhéu Grande 14.9655 −24.6768 3 777 6.7 NA 97
Fogo 14.9283 −24.3843 476 725 18 0.21 2,829
Brava 14.8515 −24.7055 64 716 18 0.5–1.99 976
Islands are ordered according to their North-South latitude. Latitude and longitude refers the centroid of the islands. NA indicates unavailable information on the geological
age; when there is no concrete date for the emergence of an island, data on geological age was represented as an interval of the most probable values. Ma and asl
indicate Millions of years and Above sea level, respectively.
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FIGURE 2 | Percentage of native species of several taxonomic groups that are endemic species of each Macaronesian archipelago (Azores, Madeira, Selvagens,
Canary Islands, and Cabo Verde) at (A) the terrestrial and (B) the marine realms. Information on the terrestrial biota was extracted from Arechavaleta et al. (2005),
Borges et al. (2008, 2010),Miralles et al. (2011),Vasconcelos et al. (2012b, 2020), and Biodiversity Data Bank of the Canary Islands (2021). Data on marine taxa was
extracted from Freitas et al. (2019) and Neto et al. (2021a,b,c), and unpublished data from one of the authors (Ávila, S.P.) regarding bivalves. The proportion of the
endemic species was calculated over the number of native species, which included those considered probably or possibly native. Only extant species and breeding
birds were considered. Lichens s.l. includes lichenicolous fungi, Vascular plants include Spermatophyta, ferns, and fern allies, Arthropods include Tardigrada, and
Crustacea only refers Brachyura (crabs). The dotted area in the bar of the Azorean Molluscs indicates the existence of some uncertainty regarding the proportion of
endemic species (43–91%; Frias Martins, A., pers. comm). In the case of Madeira, we have considered 25 additional species that have recently been classified as
native based on fossil evidence; Teixeira, D., pers. comm.). Diatoms and amoebae are not represented because of their incomplete information. Also,
Platyhelminthes (flatworms) and Annelids show the same value in Madeira and Selvagens because the source literature does not discriminate between the two
archipelagos. No data was reported for the Platyhelminthes, Nematoda (roundworms) and Annelida in Cabo Verde, and for Nematoda and crustaceans Brachyura
(crabs) in Selvagens (see ESM1 in Supplementary Material for detailed information).
and aquatic ecosystems (Malmqvist et al., 1995;Triantis et al.,
2010;Raposeiro et al., 2017;Lamelas-López et al., 2021). Marine
ecosystems are also affected by similar anthropogenic pressures,
mainly through overexploitation of biological resources (Martins
et al., 2008, 2012) and increasing urbanisation of coastal
areas (Cacabelos et al., 2016a,b;Martins et al., 2016). Climate
change also represents a threat to Macaronesian diversity, as
indicated by studies modelling the distribution of endemic
and native bryophytes, vascular plants, and arthropods under
different scenarios of climate change (Ferreira et al., 2016;
Patiño et al., 2016).
The outstanding biodiversity of the Macaronesian
archipelagos, together with the geographical, environmental
and historical idiosyncrasies of their islands have fuelled a
continuously increasing number of ecological, evolutionary,
and conservation studies. Here, we review the most important
findings of Macaronesian studies and identify further challenges
in island biology that can be addressed in this insular system.
HISTORY AND ORIGIN
Young Lineages Instead of Tertiary
Relicts
Macaronesia has primarily been defined as a biogeographical
region based on its terrestrial flowering plant species. Engler
(1879) suggested that the Macaronesian flora was mostly a
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relict of a formerly widespread subtropical flora covering
southern Europe and North Africa during the Palaeogene and
Neogene. Increasing evidence from dated phylogenies suggests
that Macaronesian endemics are often much younger than the
age of emergence of the islands they inhabit, casting doubts
on Engler’s hypothesis [e.g., vascular plants (Jones et al., 2014;
Kondraskov et al., 2015), bryophytes (Patiño and Vanderpoorten,
2015), birds (Illera et al., 2012, 2016;Valente et al., 2017),
spiders (Planas and Ribera, 2014), beetles (Emerson et al., 1999;
Amorim et al., 2012), lichens (Sérusiaux et al., 2011), reptiles
(Romeiras et al., 2019), and marine gastropods (Duda and Rolán,
2005;Baptista et al., 2019)]. Even the iconic Macaronesian
laurel forest, long viewed as an assemblage of Tertiary relictual
and palaeoendemic elements (see Fernández-Palacios et al.,
2011) may be composed of mainly young and recent colonisers
(Kondraskov et al., 2015). This pattern coincides with other
archipelagos, for example New Caledonia, with a biota mainly
formed by recent clades, despite being the oldest oceanic island
in the world (Nattier et al., 2017). However, the complex
geological dynamics of Macaronesia has led to the emergence and
disappearance of several (palaeo-)islands (Fernández-Palacios
et al., 2011), which could have served as stepping-stones
and refugia for the persistence of older lineages, as in other
archipelagos (Heads, 2010). Nevertheless, phylogenetic evidence
for the persistence of “living fossils,” whose origin predates their
native islands, is extremely rare and limited to very few species
(e.g., the moss Hedenasiastrum percurrens;Aigoin et al., 2009).
Long- and Short-Distance Dispersal in
Macaronesia
The ancestors of most extant Macaronesian lineages had to
overcome the long distances that separate the islands from the
mainland. Accordingly, many Macaronesian plants (e.g., Patiño
et al., 2013;García-Verdugo et al., 2019), lizards (Carranza
et al., 2000) and marine molluscs (e.g., Ávila et al., 2012;Faria
et al., 2017) show some adaptations to long distance dispersal
(LDD). However, there is also evidence from the Azorean flora
indicating that many plant species lack traits related to LDD
(Heleno and Vargas, 2015), and that species ability to track its
climatically suitable areas within an island is not strongly related
with LDD syndromes (Leo et al., 2021). Notably, non-standard
LDD mechanisms poorly evaluated in island systems have
been described for Macaronesia. These include secondary seed
dispersal mediated by predatory birds feeding on frugivorous
birds and lizards, which carry seeds in their digestive system
(Nogales et al., 2012;Padilla et al., 2012;Viana et al., 2016; but
see Grant et al., 1975, regarding the Galápagos), and dispersal
through mega-landslides (García-Olivares et al., 2017).
Colonisation and establishment of many plants is mediated by
generalist seed dispersers. In the Canary Islands and Madeira,
such a function is widely performed by frugivorous lizards
(Sadek, 1981;Valido and Nogales, 1994;Nogales et al., 2016;
Pinho et al., 2018), following a pattern common in many islands
worldwide (Hervías-Parejo et al., 2019;Valido and Olesen, 2019).
Lizard-plant interactions result in a relatively short-distance
dispersal pattern of seed distribution, with the lizard Gallotia
stehlini dispersing seeds over almost 100 m on Gran Canaria
(Pérez-Méndez et al., 2016). In contrast, birds can disperse viable
seeds over short and long distances within and between islands
(Nogales et al., 2001;López-Darias and Nogales, 2016).
Macaronesia as Refugium and Source of
Biodiversity for the Adjacent Mainland
Due to their buffered climate and larger sizes during glacial
periods, oceanic islands were traditionally considered as sinks
for continental terrestrial biotas (Wilson, 1961). However, a
growing body of phylogenetic evidence suggests that islands
also act as sources of continental diversity (Jønsson and Holt,
2015). Macaronesia has acted as both refugium (Vargas, 2007;
Caujapé-Castells, 2011;Fernández-Palacios et al., 2011) and,
at least to a certain extent, as a source of de novo species
for neighboring continental regions (Patiño et al., 2015). Back-
colonisation from islands to continental areas, from which the
island ancestors originated (“boomerang events” sensu Caujapé-
Castells, 2011), was first postulated by Ball and Hooker in
1878 for Macaronesia (Fernández-Palacios and Whittaker, 2020),
and more than a century later was confirmed for the genera
Aeonium (Mort et al., 2002) and Convolvulus (Carine et al., 2004).
Further evidence derives from bryophytes and spermatophytes
(e.g., Fernández-Mazuecos and Vargas, 2011;Hutsemékers et al.,
2011), and beetles (Machado et al., 2017). Similar processes
have later been described in New Zealand and New Caledonia
(Condamine et al., 2017). The close proximity of some of the
Macaronesian islands (Canary Islands and Cabo Verde) to their
continental species pools, the changes in island surface area,
isolation and predominant wind and ocean currents through
time, together with the emergence of seamounts during glacial
periods (Fernández-Palacios et al., 2011;Rijsdijk et al., 2014)
may have allowed even greater connectivity between these
landmasses in the past.
High or Reduced Genetic Diversity of
Island Populations?
The few individuals that successfully arrive and colonise
islands carry just a subset of the genetic variation in the
parental continental populations (Frankham, 1997;Clegg, 2010).
In Macaronesia, isolation after colonisation seems to have
driven both genetic and phenotypic divergence in Berthelot’s
pipit (Anthus berthelotii), and not geographical distance or
environmental differences (Spurgin et al., 2014). In contrast,
Stuessy et al. (2012) suggested that genetic signatures of founder
effects rarely persist over evolutionary time-scales in island
plants. Indeed, a growing body of empirical evidence for
Macaronesian bryophytes and angiosperms suggests that genetic
diversity is often substantially higher than in the continental
source populations (Fernández-Mazuecos and Vargas, 2011;
Laenen et al., 2011;Desamoré et al., 2012;García-Verdugo
et al., 2015;Patiño et al., 2015). Strikingly, the invasive house
mouse (Mus musculus domesticus) in Madeira also follows this
pattern. Evidence supports an initial introduction event about
one millennium ago (Förster et al., 2009;Rando et al., 2014),
with subsequent in situ genetic diversification that resulted in
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six chromosomal races distributed around the island (Britton-
Davidian et al., 2000). This rapid diversification can be explained
by meiotic drive due to a biased segregation of chromosomes
to oocytes during female meiosis. The underlying biological
mechanism involves differential centromere strength (a trait with
natural variation among populations), predicting the direction of
drive (Chmatal et al., 2014). This can result in the rapid fixation
of distinct chromosomal combinations and, consequently, an
increase in genetic diversity.
COMMUNITY ECOLOGY IN
MACARONESIA
After arrival on islands, ecological processes act as major
drivers of island community assembly, along with speciation
and extinction events (Figure 3). MacArthur and Wilson
(1963, 1967) highlighted the dynamic nature of the processes
leading to community composition changes through time.
Since not all species are equally likely to colonise islands,
one general assumption is that island biotas are impoverished
and taxonomically “imbalanced”—a phenomenon known as
disharmony—when compared to adjacent mainland regions. As
a consequence of this “vacant ecological space,” some species
might have the opportunity to broaden, or even shift their niche
width through “ecological release” (Diamond, 1970). Prominent
examples are the Azorean endemic bat Nyctalus azoreum, which
exhibits the rare behaviour of being active during the day,
probably due to the absence of avian competitors or predators
(Moore, 1975; see Chua and Aziz, 2018, for a similar case in
Malaysia). The Cabo Verde giant gecko Tarentola gigas, which
preys on birds (Pinho et al., 2018) in the absence of mammalian
top predators, is another example. Ecological release also occurs
in different Macaronesian insect groups, in both terrestrial
(Ribeiro et al., 2005;Stüben et al., 2010;Santos et al., 2011) and
aquatic ecosystems (Raposeiro et al., 2012).
Mutualistic Interactions
Species interactions associated with pollination and seed-
dispersal processes can influence large-scale biodiversity patterns.
In insular systems, pollination networks commonly show
distinctive and idiosyncratic ecological characteristics known as
insular pollination syndromes (Valido and Olesen, 2010). For
example, in the Canary Islands, generalist lizards and birds are
important pollinators and seed dispersers (Valido et al., 2004;
Valido and Olesen, 2010, 2019;Hernández-Teixidor et al., 2019),
an uncommon behaviour in mainland systems (Olesen and
Valido, 2003). Notably, Macaronesian pollinators tend to visit
a wider range of plant species than their mainland relatives
(“interaction release” sensu Traveset et al., 2015).
These particularities of island mutualistic networks suggest
they may be notably vulnerable to similarly particular
disturbances (see Heleno et al., 2013;Traveset et al., 2013
for Galápagos). González-Castro et al. (2012) compared the
seed dispersal network structure of thermophilous woodland on
Tenerife (Canary Islands) to mainland woodland and found that
the lower number of species and greater specialisation on the
island led to the prevalence of more symmetrical interactions,
compared to the mainland. Also, Nogales et al. (2016)
demonstrated that Canarian seed dispersal networks are
highly nested (stable against disassembly) but weakly modular
(the ensemble of species that interact more intensively), and
therefore highly vulnerable to extinction cascades.
Alien Species
The introduction of alien species is one of the main threats to
biodiversity in Macaronesia and worldwide. More than 70% of
vascular plants and more than 50% of arthropod species in the
Azores are aliens (Silva et al., 2008). Especially successful invaders
in Macaronesia include the plants Cenchrus spp., Hedychium
gardnerianum, Pittosporum undulatum and Ulex europaeus,
as well as vertebrates like cats (Felis sylvestris), goats (Capra
hircus), Corsican mouflons (Ovis aries musimon), Barbary sheep
(Ammotragus lervia), rats (Rattus rattus and R. norvegicus), house
mice (Mus musculus domesticus), rabbits (Oryctolagus cuniculus),
and Californian kingsnakes (Lampropeltis californiae). The
spread of alien fish in the absence of native predators is
an important threat to freshwater systems in Macaronesia
(Ribeiro et al., 2009), impacting trophic cascades and ecosystem
functioning (Skov et al., 2010;Buchaca et al., 2011;Raposeiro
et al., 2017). A high number of alien species have been also
reported in the marine realm of Macaronesia, with shipping as the
most likely vector of these introductions (Chainho et al., 2015).
Schaefer et al. (2011) found that for the Azorean flora, alien
species that are phylogenetically distant from native species
are more likely to become invasive, corroborating Darwin’s
naturalisation hypothesis. Moreover, Padrón et al. (2009) and
Picanço et al. (2017) showed that endemic and native super-
generalist pollinators included new plant invaders in their set
of food plants and thereby may help the establishment of alien
and invasive plants. Indeed, alien bees pollinate most of the
endemic Azorean flora (Weissmann et al., 2017). However,
domestic honeybees (Apis mellifera) disrupt the structure
and functionality of the plant-pollinator networks in Teide
National Park (Tenerife, Canary Islands), reducing diversity
and interaction links among wild pollinators, their hierarchical
organisation, and the reproductive success of some endemic
plants (Valido et al., 2002, 2019;Dupont et al., 2004). Also, alien
arthropods added novel trait space in the Azores (Whittaker
et al., 2014), and might play important roles in providing
and maintaining some key ecosystem functions, particularly in
anthropogenic systems such as cattle pastures (Rigal et al., 2018).
SPECIATION, DIVERSIFICATION, AND
EXTINCTION IN MACARONESIA
Ecological opportunities on islands may foster diversification and
speciation processes. New ecological opportunities are created
when new habitats become available, such as subterranean
environments that emerge as a consequence of present
and/or past volcanic activity. For example, many phylogenetic
and phylogeographical studies on endemic radiations of the
Macaronesian arthropods include troglobiont species, such as
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FIGURE 3 | Processes leading to community assembly in island biotas. The grey arrow represents dispersal from the species pool since historical times (t=n).
Species able to colonise an island are subject to several processes and factors acting at the regional and local scales (some examples of these are indicated inside
the two green arrows conforming a circle), which can lead to community assembly (large green arrow) and to the current biodiversity on islands (green box;
t=n+1). The extant island biodiversity is a result of speciation and diversification under regional and local abiotic constraints and biotic interactions. Current island
assemblages and biodiversity are affected by anthropogenic disturbances such as environmental changes, species introductions and land-use changes (red arrows)
that can lead to extirpation of species (red box), and are thus often targeted by conservation actions (green dashed box).
Dysdera spiders (Arnedo et al., 2007), Palmorchestia sandhoppers
(Villacorta et al., 2008), Trechus ground beetles (Amorim, 2005;
Contreras-Díaz et al., 2007), and Laparocerus weevils (Machado
et al., 2017). Examples of radiations known to be adaptive are
found among flowering plants (e.g., Echium—García-Maroto
et al., 2009;Aeonium—Jorgensen and Olesen, 2001;Mort et al.,
2001) and reptiles (e.g., Gallotia—Cox et al., 2010;Tarentola—
Carranza et al., 2000;Vasconcelos et al., 2010). These taxa
correspond to examples of diversification events associated with
niche lability, in which closely related species present contrasting
niches. Such niche differentiation can be reflected in current
species distribution, as occurs in some plant clades in the
Canary Islands, where closely related taxa present different
climatic niches, particularly in allopatry (Steinbauer et al., 2016).
However, not all diversification processes have arisen from
changes in species niches; niche conservatism, which can be
described as the tendency for ancestral niche and ecological
characteristics to remain unchanged through time and space
(Wiens and Graham, 2005), has also been an important speciation
outcome in different taxa (e.g., Helianthemum—Albaladejo et al.,
2021). Notably, the flora of the Azores is characterised by a
limited incidence of adaptive radiations, contrasting with other
Macaronesian archipelagos (Carine and Schaefer, 2010); the
debate about the drivers of this pattern has pinpointed past
climatic conditions, age, area and environmental homogeneity
as the most plausible causes (Carine and Schaefer, 2010;Carine
et al., 2012;Triantis et al., 2012).
Species interactions could also have fuelled species
diversification in Macaronesia. By combining morphological
data, radiocarbon dating, and molecular data, Rando et al. (2010)
recovered an ecological interaction (resource competition)
between sympatric extinct and extant finches of Tenerife for
approximately 1 Ma. This interaction led to variations in bill
size, as more famously known from the Galápagos finches
(Grant and Grant, 2006). The presence on other Macaronesian
islands of other extinct granivorous birds with significant
variation in bill size suggests that character displacement
between extinct and extant birds frequently occurred, to
minimise competition for food (Rando et al., 2010).
The interaction between dispersal limitations and geological
dynamics as drivers of diversification has attracted increased
attention (Anderson et al., 2009;Fernández-Palacios et al.,
2011;Rijsdijk et al., 2014;Ávila et al., 2015a). A history
of massive landslides and their associated mega-tsunamis
in Macaronesia allowed this question to be addressed at
the within-island level (cf. Paris et al., 2018). Studies on
endemic lizards and beetles point to an important role of
these geological events in shaping the genetic structure of
endemic lineages (Brown et al., 2006;García-Olivares et al.,
2017) and, in combination with past climate oscillations, the
community-wide diversification patterns across beetle species
over a limited spatial scale (Salces-Castellano et al., 2020).
Lava flows, that appear during volcanic activity, have led to
population extirpation and the appearance of dispersal barriers,
greatly affecting phylogeographic patterns and speciation (e.g.,
Gallotia—Bloor et al., 2008). The dynamics of sea-level changes,
particularly those that occurred in the Quaternary, have affected
island area, isolation and connectivity, which consequently
influenced migration, extinction, and speciation, leaving an
important imprint in current island richness, particularly of
endemic species (Fernández-Palacios et al., 2011;Rijsdijk et al.,
2014;Weigelt et al., 2016). As a consequence, Lanzarote and
Fuerteventura, two islands that were connected in the Last
Glacial Maximum (∼18,000 years ago), share more insect and
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plant species than any other islands within the Canary Islands
(Fernández-Palacios et al., 2011;Rijsdijk et al., 2014), and
in Cabo Verde, only Tarentola spp. that occurred on islands
connected during this period share haplotypes (Vasconcelos
et al., 2010). Such dynamics also affected marine diversity, for
example through its effects on sea-surface currents and dispersal
routes (e.g., Ávila et al., 2009;Sousa et al., 2021), and on
the characteristics of the intertidal zone (Ávila, 2013). Recent
palaeocological studies have related marine ecological traits (e.g.,
the substrate where animals live) with extirpation/extinction
trends, putting in evidence the impact of sea-level changes
on insular shallow-water benthic marine communities (Ávila
et al., 2009). Also, species range contractions and extensions
(e.g., Persististrombus spp. and Conus spp., respectively; Meco
et al., 2002;Ávila et al., 2015a, 2016) have been documented,
and show the impact of climatic global changes associated
with Pliocene climatic deterioration and the abrupt Pleistocene
glacial/interglacial transitions (the so-called “Terminations”) on
species distributions.
Extinction in Macaronesia
Natural extinctions have been driven by ancient changes in
climate and habitat. Oxygen isotope data suggest that most of
the Pliocene marine fauna of the Azores became extinct 3.6–3.3
Ma ago as a result of glaciation (Ávila et al., 2015b, 2016;Santos
et al., 2015). In addition, volcanism and geological catastrophes
such as massive landslide events and mega-tsunamis, can also
act as important drivers of island-wide natural extinction events
(Anderson et al., 2009). However, human arrival has greatly
impacted island biotas, accelerating species extinctions on islands
(e.g., Triantis et al., 2010;Russell and Kueffer, 2019) to the point
of influencing our understanding of basic evolutionary patterns
(e.g., body size evolution toward dwarfism or gigantism on island
species; Faurby and Svenning, 2016).
Canarian giant lizards (Gallotia spp., Lacertidae) underwent
a strong defaunation process after human colonisation, with
negative consequences on the seed dispersal distances and genetic
variation of endemic plants, such as Cneorum (Neochamaelea)
pulverulentum (Pérez-Méndez et al., 2018). Palaeobiological
evidence also points to the extinction of several other species
after human arrival, such as most flightless or weak-flying
ground-nesting Canarian birds, as suggested by radiocarbon
dating of bone collagen (Illera et al., 2016). In total, more
than 20 endemic and many non-endemic vertebrate species that
lived during the Upper Pleistocene-Holocene became extinct in
Macaronesia, such as the iconic Cocteau’s giant skink of Cabo
Verde or the Macaronesian rails species (Vasconcelos et al.,
2013;Alcover et al., 2015;Rando et al., 2020). Long-term fossil
pollen and charcoal records have shown a decline in native plant
diversity (possibly including some tree genera now absent as
natives on Tenerife such as Quercus and Carpinus), introduction
of non-native forest species (e.g., Cryptomeria japonica and
Pinus pinaster in the Azores), and an increasing rate of fire
occurrence after human arrival (de Nascimento et al., 2009, 2016;
Gabriel et al., 2015;Rull et al., 2017). In the marine realm,
the overexploitation of biological resources, such as the case of
limpets, crustaceans and fishes, may also cause the extirpation of
keystone species in coastal trophic chains (Navarro et al., 2005;
Martins et al., 2008, 2010).
BIODIVERSITY PATTERNS AND MODELS
Species Distributions
Species abundance distributions (SADs), which are key
descriptors of community structure, have been little investigated
in island empirical studies (but see Ulrich and Zalewski, 2006,
for lake islands, and Garcillán and Ezcurra, 2011, regarding
Guadalupe Island, Baja California). In Macaronesia, Azorean
arthropod communities are dominated by a few highly abundant
single-island endemic species that may be assumed to be well
adapted to specific island environmental conditions (Fattorini
et al., 2016). These SADs of the Azorean arthropods follow
a power law pattern when plotted according to sample size,
which is similar to that observed for tropical tree SADs; this
might indicate a general pattern in ecology (Borda-de-Água
et al., 2017). Considered as one of the most general patterns
in nature, the island species-area relationship (ISAR) has been
widely studied using data from many archipelagos, namely those
pertaining to Macaronesia (e.g., Cardoso et al., 2010;Santos
et al., 2010;Aranda et al., 2013). Although the ISAR has mostly
been studied in terrestrial systems, interest in evaluating it in
marine and other aquatic systems is growing (Dawson, 2016).
As an example in the marine realm, Tuya and Haroun (2009)
found that intra-archipelago differences in species richness of
Macaronesian macroalgae are largely related to variations in
island perimeter (a proxy for island area).
The General Dynamic Model of Oceanic
Island Biogeography
Islands are dynamic entities that have undergone climatic
and geological changes through time. The General Dynamic
Model of oceanic island biogeography (GDM; Whittaker et al.,
2008;Borregaard et al., 2017) considers the effect of geological
dynamics of oceanic islands on their diversity. The GDM has
been intensively tested in Macaronesia, namely with arthropods
(Borges and Hortal, 2009;Cardoso et al., 2010), reptiles
(Vasconcelos et al., 2010), snails (Cameron et al., 2013), and
bryophytes (Patiño et al., 2013;Aranda et al., 2014), and also
in the sea (Ávila et al., 2018). While these evaluations show the
potential of the GDM for predicting patterns of island species
richness through time, they also pinpoint the need to account for
island and taxon particularities when applying biogeographical
models (see Borges and Hortal, 2009). The third component of
the original theory of island biogeography, geographical isolation,
was only recently included within the GDM framework, with
Macaronesia (and Hawaii) being used as testing grounds (Patiño
et al., 2013;Carvalho et al., 2015).
Recent studies on Macaronesian islands showed that the
hump-shaped relationship between species richness and
island geological age also holds for network interactions
and genetic diversity, in which island age and dynamics act
as regional drivers of plant-pollinator network complexity
(see Trøjelsgaard et al., 2013 for an example in the Canary
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Islands). Similarly, Vasconcelos et al. (2010) showed that
volcanism and habitat diversity appear to be the main factors
explaining the genetic diversity of Tarentola geckos in Cabo
Verde, since they are both tightly linked with island ontogeny
as postulated by the GDM. The importance of island age for
explaining diversity patterns is also present in the marine realm.
On a broader Atlantic archipelagos’ context, Hachich et al. (2015)
found a linear relationship between reef fish diversity and island
age. More recently, Fernández-Palacios et al. (2016) developed a
Glacial Sensitive Model (GSM) of oceanic island biogeography
partially based on Macaronesian islands, which includes the
role of glacial and interglacial periods in the GDM. Building
on these models, Ávila et al. (2019) developed the Sea-Level
Sensitive dynamic model (SLS) of marine island biogeography.
This model offers predictions on how immigration, colonisation
and in situ speciation rates affect marine biodiversity around
oceanic islands.
NATURE CONSERVATION IN
MACARONESIA
Several political, scientific and social initiatives toward
improving conservation practices and public awareness
have been established in Macaronesia. For example, the cost-
effectiveness of conservation and governance policies can be
improved by relying on island ecosystem-based management
(Calado et al., 2016;Gil et al., 2016a), stakeholder engagement
and public participation (Gil et al., 2011, 2016b), and funding
to support and strengthen ecosystem functions and services
delivery (e.g., Cruz et al., 2011;Fernandes et al., 2015). Hence, the
last decade has witnessed the publication of important studies
aiming to assist local and regional decision-making systems in
moving toward more effective nature conservation planning
and management policies in Macaronesia. Special attention has
been given to “Natural Protected Areas” design and effectiveness
(Vergílio et al., 2016;Gil et al., 2017). Several indices for the
selection of priority areas for conservation have been developed
based on Macaronesia (Gaspar et al., 2011;Borges et al., 2012;
Cardoso et al., 2013). An innovative, cost-effective and replicable
methodology has also been developed for protecting genetic
diversity in reserves (Vasconcelos et al., 2012a). Furthermore,
knowledge gathered in Macaronesia has been also used to
propose several methodologies and standardised protocols
for conservation assessment of endemic species (Borges et al.,
2018). Identifying top-priority species is particularly useful for
designing conservation strategies. However, applying IUCN
criteria (IUCN Standards and Petitions Subcommittee, 2017) to
oceanic islands may have serious shortcomings (Martín, 2009;
Cardoso et al., 2011;González-Mancebo et al., 2012), leading,
for example, to assigning species to higher threat categories
(Romeiras et al., 2016a). Therefore, species risk tolerance should
be adjusted within island systems (Romeiras et al., 2016b).
Macaronesia also served as the basis for developing successful
innovative approaches for alien species management on islands,
including prevention, early detection, eradication and control
of invaders, as well as proper legislation. For instance, a list
of the priority TOP 100 invasive alien species in Macaronesia
has been compiled (Silva et al., 2008), based on their known
impacts upon native and endemic biodiversity and the feasibility
of successful control. Furthermore, the Canary Islands, Madeira
and Selvagens have provided examples of successful eradication
and control schemes for rabbits, cats, mice, and plants (e.g.,
Bell, 2001;Olivera et al., 2010). In the Azores, a regional
programme to control invasive alien plants in sensitive areas
has revealed the importance of maintenance to prevent alien
regrowth (Costa et al., 2013).
Several initiatives and programmes have led to the successful
restoration of different endemic and native species. One
emblematic threatened species in Macaronesia is the Azorean
endemic bullfinch (Pyrrhula murina), a species that has recovered
through habitat restoration and removal of alien species (“LIFE
Priolo” project; SPEA, 2006); such actions have led to positive
impacts not only on the target species, but also on native
plants, insects and birds (Heleno et al., 2010). The giant
lizard Gallotia simonyi and the Raso lark Alauda razae are
other threatened endemic species that have been the target
of strong conservation actions, like breeding programmes and
reintroductions in small islets and islands of the Canary
Islands and Cabo Verde, respectively (Salvador, 2015;Brooke
et al., 2020); recent innovative actions that will enhance future
reintroductions of the giant lizards, include training procedures
where individuals raised in captivity learn to avoid predators
(Burunat-Pérez et al., 2018).
MACARONESIA AND FUTURE
PROSPECTS IN ISLAND BIOLOGY
We have highlighted a large number of research questions
addressed using Macaronesia as a natural laboratory. The
comprehensive ecological and evolutionary datasets gathered
so far in different studies have already proven essential for
current understanding of island biology. Unfortunately, many
extant and extinct species still remain undescribed and some
environments underexplored (e.g., subterranean, marine), and
thus our knowledge is far from complete in Macaronesia (Lobo
and Borges, 2010). More efforts should be made toward gathering
basic information on species taxonomy, distribution, abundance,
evolution and ecology. Still, there are many research avenues
to be explored (e.g., Santos et al., 2016;Patiño et al., 2017),
and below we point out the importance of these archipelagos
for pursuing them.
The proximity of some Macaronesian islands to the adjacent
mainland provides a well-suited geological set-up for island-
mainland comparisons, for instance to evaluate genetic diversity,
gene-flow patterns and the importance of islands in generating
mainland diversity. The genetic imprints of founder events and
the impact of historical geological and climatic events (or their
absence) can be tested with the increasing number of locally
relevant population genetics and genomic datasets available,
and applying approaches based on multitaxon comparisons
that could help understand how much biotic interchange has
occurred not only between islands and the mainland, but also
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between archipelagos (see e.g., Antonelli et al., 2018). Although
ecological opportunities are considered as potential drivers of
the remarkable radiations that occurred in the region, the degree
to which isolation affects such speciation processes is still not
entirely understood (Patiño et al., 2017). The combination of
phylogenetic information and trait data that are increasingly
becoming available in this region will allow understanding the
processes behind niche evolution, particularly how labile and
conserved ecological attributes, together with the availability
of novel habitats, affect speciation and lineage diversification
(see Edwards and Donoghue, 2013). The unique subterranean
ecosystems and fossiliferous outcrops of Macaronesia are
windows into past insular terrestrial and marine biotas, providing
opportunities to evaluate the role of vacant ecological space,
trait lability and isolation on diversification and speciation.
Island-mainland comparisons can also be extended to different
ecological questions, namely those related with the processes
leading to community assembly and rarity (e.g., Santos et al.,
2011;Borda-de-Água et al., 2017;Boieiro et al., 2018). Future
research could therefore focus on comparing species-abundance
distribution patterns between the two settings in order to
understand the generality of such relationship (e.g., following,
Borda-de-Água et al., 2017), or contrasting islands and mainland
trait and phylogenetic diversity to ascertain which are the
driving forces of community assembly (e.g., habitat filtering
vs. competition; e.g., Santos et al., 2016). Another interesting
and related topic is the study of the biodiversity-ecosystem
functioning relationship; island-mainland comparisons can also
be useful for understanding how systems with different species
richness and trait diversity can provide the basic ecosystem
services on which humans depend.
Research conducted in Macaronesia has been pivotal in
understanding island mutualistic interactions. Further studies
on interaction networks will shed new light onto how biotic
interactions affect community assembly, immigration, and
extinction on islands, and on how alien species become integrated
into the receptive communities and impact species interactions.
Further studies from other archipelagos will also confirm whether
the network patterns found for the Macaronesian islands are
general or rather idiosyncratic (first comparisons with the
Galápagos suggest these patterns are not general). Evaluating
how such patterns may have influenced colonisation/extinction
dynamics or speciation rates are prominent avenues that
might change our understanding of island biogeography
(Nogales et al., 2016).
Some of the most pressing questions in current research
agendas are linked to the impact of global change on biodiversity
patterns and processes as well as on human well-being. Such
efforts are devoted to developing management strategies that can
safeguard biodiversity and ecosystem services (Butchart et al.,
2010). The relatively well-known history of human settlement
across the islands and associated land-use transformations aids
in assessing the relative impacts of environmental (pre)historical,
demographic, and socioeconomic changes on current island
biodiversity (see for instance: Nogué et al., 2013, 2017, 2021;
Norder et al., 2020). Alien species constitute one of the most
important threats island biotas face (Russell and Kueffer, 2019).
The simplified nature of island biotas might be essential for
understanding how newly arrived species establish and affect
existing species and ecosystems, and the implications of these
novel species in conservation strategies. However, the precise
impacts of novel native-alien interactions on island biodiversity
and ecosystem functioning are still unclear (Patiño et al., 2017).
Indeed, Lundgren et al. (2020) found that alien mammalian
herbivores seem to have replaced some ecological functions that
would otherwise be lost through the anthropogenic extinction of
native species, a pattern that might not be extended to all island
communities (e.g., Sobral et al., 2016). Long-term ecological data
(see Van Leeuwen et al., 2005;Nogué et al., 2017) provide essential
clues to disentangle the colonisation status of insular species and
will contribute to progress in this research agenda.
CONCLUSION
Macaronesia has played a crucial role in the development of
island biology. Research contributions in this region provide
insights into ecological and evolutionary theories tested for
other archipelagos (e.g., the General Dynamic Model of oceanic
island biogeography, and its subsequent updates). Furthermore,
political, scientific and social initiatives launched in Macaronesia
to improve conservation practices and public awareness can
be implemented in other regions, to assure the maintenance
of biodiversity. However, knowledge of Macaronesia diversity
is far from complete, and it is essential to continue gathering
reliable data about species distribution to understand the
relative importance of spatial, historical and ecological processes.
Therefore, initiatives like long-term diversity studies need to be
continued in Macaronesia, to obtain high quality data that will
allow to widen knowledge of island biology in general.
DEDICATION
This article is dedicated to the memory of our co-author, Ana I.
Neto. May she rest in peace.
AUTHOR CONTRIBUTIONS
MF led the manuscript writing, with significant contributions
from AMCS, JP, SN, AT, PB, and HS. IRA led the subterranean
biology group composed of PB, PC, PO, MA, and AM. RH led
the marine biology group: AN, SÁ, and GM. AMCS led the
community ecology group: JF-P, PB, and FR. PB led the biological
conservation group composed of AG and RV. JP led the evolution
group, comprising JCI, MR, HS, AVan, MA, and SG. MF led the
freshwater biology group: PR and VG. AT led the plant-animal
interaction and long-distance dispersal group: MN and AVal. MF
led the biological invasion group: ML-D, LS, and MN. PB led
the macroecology group, aided by PC. SN led the palaeobiology
group: SÁ, JF-P, LN, and JR. All authors contributed to the drafts
and gave final approval for publication.
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FUNDING
This research has been partially funded by the project
REMEDINAL TECM (S2018/EMT- 4338). MF was funded
by the Conselho Nacional de Desenvolvimento Científico e
Tecnológico—CNPq (401045/2014-5) programme “Ciência
sem Fronteiras,” and the University of Alcalá, being currently
funded by the Universidad Autónoma de Madrid. MF is
also grateful to the project ClimaRiskinPond (PID2019-
104580GA-I00/AEI/10.13039/501100011033) funded by the
Spanish Ministry of Science and Innovation. PB is grateful
to the projects MACDIV (FCT-PTDC/BIABIC/0054/2014)
and MOMENTOS (FCT-PTDC/BIA-BIC/5558/2014), funded
by the Portuguese “Fundação para a Ciência e a Tecnologia,
I.P” (FCT). AMCS and JP were supported by a Juan
de la Cierva—Incorporación Fellowship (IJCI-2014-19502
and IJCI-2014-19691, respectively) funded by the Spanish
“Ministerio de Ciencia, Innovación y Universidades.” AMCS
was additionally supported by a Marie Curie Intra-European
Fellowship (IEF 331623 “COMMSTRUCT”), and by FCT
(contract CEEIND/03425/2017). JP was additionally supported
by a Ramón y Cajal Programme (RYC-2016-20506) and a
Marie Skłodowska-Curie COFUND, Researchers’ Night and
Individual Fellowships Global (MSCA grant agreement no
747238, “UNISLAND”). SÁ acknowledges his IF/00465/2015
research contract funded by FCT (Portugal). SÁ, LS, PR, and
VG were also funded by FEDER funds through the Operational
Programme for Competitiveness Factors–COMPETE and by
National Funds (FCT): UID/BIA/50027/2013 and POCI-01-
0145-FEDER-006821. AM was supported by Marie Skłodowska-
Curie Individual Fellowship (IF-EF), H2020 Programme of the
EU, number 745530—“ANCAVE-Anchialine caves to understand
evolutionary processes.” Attendance by JF-P and LN at the Island
Biology Conference 2016 was supported by the University of
La Laguna through the “Ayudas a Proyectos Puente al Plan
Estatal de I +D+I, Plan Propio de Investigación 2016.” LN
was supported by the European Union’s Horizon 2020 Research
and Innovation Programme under the Marie Skłodowska-Curie
grant agreement no. 700952. IRA (SFRH/BPD/102804/2014),
SG (SFRH/BPD/88854/2012), and RV (SFRH/BPD/79913/2011)
were supported by post-doc grants from FCT, financed by The
European Social Fund and the Human Potential Operational
Programme, POPH/FSE. IRA, RV, and PR were funded by
Portuguese funds through FCT, under the “Norma Transitória”—
DL57/2016/CP1375/CT0003, DL57/2016/CP1440/CT0002,
and DL57/2016/ICETA/EEC2018/25, respectively. MR was
funded by Aga Khan Development Network and FCT
(CVAgrobiodiversity/333111699). SG also thanks financial
support from FCT/MCTES for the financial support to
CESAM (UIDP/50017/2020 +UIDB/50017/2020), through
national funds and in the scope of the framework contract
foreseen in the numbers 4, 5, and 6 of the article 23, of the
Decree-Law 57/2016, of August 29, changed by Law 57/2017,
of July 19. AVal and MA were supported by the Ministerio de
Economía y Competitividad (CGL2013-47429-P and PGC2018-
099772-B-I00, and CGL2016-80651-P, respectively). MA is also
grateful to the Catalan Government (grant 2017SGR83). ML-D
also acknowledges her current contract financed by Cabildo de
Tenerife, Programme TF INNOVA 2016-21 (with MEDI and
FDCAN Funds). RH beneffited from research funds provided
by the EU ERA-Chair project EcoAqua (Grant # 621341). JCI
was funded by a research grant from the Spanish Ministry of
Science, Innovation and Universities, and the European Regional
Development Fund (Ref.: PGC2018-097575-B-I00) and by a
regional GRUPIN grant from the Regional Government of
Asturias (Ref.: IDI/2018/000151).
ACKNOWLEDGMENTS
The Island Biology Interest Group (IBIG, http://www.
ibigbiology.com) is grateful to the organisers of the 2016 Island
Biology Conference held in the Azores for promoting the
symposium that led to this manuscript. We thank Joaquin Hortal
for useful comments on an early version of the manuscript,
and also Guido Jones for his language editing funded by the
Cabildo de Tenerife, under the TFinnova Programme supported
by MEDI and FDCAN funds. We are grateful to Salvador de
la Cruz and Elena Morales for extracting updated information
from the Biodiversity Data Bank of the Canary Islands. We
also thank Ricardo Ramalho (Cardiff University) for fruitful
discussions on the geological age of the Cabo Verde islands. This
manuscript is a contribution by the INCT in Ecology, Evolution
and Biodiversity Conservation funded by MCTIC/CNPq/FAPEG
(grant 465610/2014-5).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.2021.
718169/full#supplementary-material
REFERENCES
Aigoin, D. A., Devos, N., Huttunen, S., Ignatov, M. S., Gonzalez-Mancebo,
J. M., and Vanderpoorten, A. (2009). And if Engler was not completely
wrong? Evidence for multiple evolutionary origins in the moss flora
of Macaronesia. Evolution 63, 3248–3257. doi: 10.1111/j.1558-5646.2009.00
787.x
Albaladejo, R. G., Martín-Hernanz, S., Reyes-Betancort, J. A., Santos-Guerra, A.,
Olangua-Corral, M., and Abelardo, A. (2021). Reconstruction of the spatio-
temporal diversification and ecological niche evolution of Helianthemum
(Cistaceae) in the Canary Islands using genotyping-by-sequencing data. Ann.
Bot. 127, 597–611. doi: 10.1093/aob/mcaa090
Alcover, J. A., Pieper, H., Pereira, F., and Rando, J. C. (2015). Five new extinct
species of rails (Aves: Gruiformes: Rallidae) from the Macaronesian Islands
(North Atlantic Ocean). Zootaxa 4057, 151–190. doi: 10.11646/zootaxa.4057.2.1
Amorim, I. R. (2005). Colonization and Diversification on Oceanic Islands: Forest
Tarphius and Cave Dwelling Trechus Beetles of the Azores. Ph.D. Dissertation.
Los Angeles, CA: University of California.
Amorim, I. R., Emerson, B. C., Borges, P. A. V., and Wayne, R. K. (2012).
Phylogeography and molecular phylogeny of Macaronesian Island Tarphius
Frontiers in Ecology and Evolution | www.frontiersin.org 12 November 2021 | Volume 9 | Article 718169

fevo-09-718169 November 1, 2021 Time: 13:44 # 13
Florencio et al. Macaronesia as a Research Hotspot
(Coleoptera: zopheridae): why are there so few species in the Azores? J. Biogeogr.
39, 1583–1595. doi: 10.1111/j.1365-2699.2012.02721.x
Ancochea, E., Hernán, F., Huertas, M. J., and Brändle, J. L. (2012). A basic radial
dike swarm of Boa Vista (Cape Verde Archipelago); its significance in the
evolution of the Island. J. Volcanol. Geoth. Res. 243, 24–37. doi: 10.1016/j.
jvolgeores.2012.06.029
Ancochea, E., Huertas, M. J., Hernán, F., and Brändle, J. L. (2010).
Volcanic evolution of São Vicente, Cape Verde Islands: the Praia Grande
landslide. J. Volcanol. Geoth. Res. 198, 143–157. doi: 10.1016/j.jvolgeores.2010.
08.016
Ancochea, E., Huertas, M. J., Hernán, F., Brändle, J. L., and Alonso, M. (2015).
Structure, composition and age of the small islands of Santa Luzia, Branco
and Raso (Cape Verde Archipelago). J. Volcanol. Geoth. Res. 302, 257–272.
doi: 10.1016/j.jvolgeores.2015.07.015
Anderson, C. L., Channing, A., and Zamuner, A. B. (2009). Life, death and
fossilization on Gran Canaria–implications for Macaronesian biogeography
and molecular dating. J. Biogeogr. 36, 2189–2201. doi: 10.1111/j.1365-2699.
2009.02222.x
Antonelli, A., Zizka, A., Carvalho, F. A., Scarhn, R., Bacon, C. D., Silvestro, D.,
et al. (2018). Amazonia is the primary source of Neotropical biodiversity.
Proc. Natl. Acad. Sci. U.S.A. 115, 6034–6039. doi: 10.1073/pnas.171381
9115
Aranda, S. C., Gabriel, R., Borges, P. A. V., Santos, A. M. C., Azevedo, E. B., Patiño,
J., et al. (2014). Geographical, temporal and environmental determinants of
bryophyte species richness in the Macaronesian Islands. PLoS One 9:e101786.
doi: 10.1371/journal.pone.0101786
Aranda, S. C., Gabriel, R., Borges, P. A. V., Santos, A. M. C., Hortal, J., Baselga,
A., et al. (2013). How do different dispersal modes shape the species–area
relationship? Evidence for between-group coherence in the Macaronesian flora.
Glob. Ecol. Biogeogr. 22, 483–493. doi: 10.1111/geb.12008
Arechavaleta, M., Rodríguez, S., Zurita, N., and García, A. (2010). Lista de Especies
Silvestres de Canarias. Hongos, Plantas y Animales Terrestres 2009. Santa Cruz
de Tenerife: Gobierno de Canarias.
Arechavaleta, M., Zurita, N., Marrero, M. C., and Martín, J. L. (2005). Lista
Preliminar de Especies Silvestres de Cabo Verde (Hongos, Plantas y Animales
Terrestres). Santa Cruz de Tenerife: Gobierno de Canarias.
Arnedo, M. A., Oromí, P., Múrria, C., Macías-Hernández, N., and Ribera, C.
(2007). The dark side of an island radiation: systematics and evolution of
troglobitic spiders of the genus Dysdera (Araneae, Dysderidae) in the Canary
Islands. Invertebr. Syst. 21, 623–660. doi: 10.1071/IS07015
Ávila, S. P. (2013). “Unravelling the patterns and processes of evolution of marine
life in oceanic islands: a global framework,” in The Climate Change Perspectives
from the Atlantic: Past, Present and Future, eds J. M. Fernández-Palacios, L. De
Nascimento, J. C. Hernández, S. Clemente, A. González, and J. P. Díaz-González
(Tenerife: Universidad de La Laguna), 95–125.
Ávila, S. P., Cordeiro, R., Madeira, P., Silva, L., Medeiros, A., Rebelo, A. C., et al.
(2018). Global change impacts on large-scale biogeographic patterns of marine
organisms on Atlantic oceanic islands. Mar. Pollut. Bull. 126, 101–112. doi:
10.1016/j.marpolbul.2017.10.087
Ávila, S. P., Goud, J., and Martins, A. M. F. (2012). Patterns of diversity of the
Rissoidae (Mollusca: gastropoda) in the Atlantic and the Mediterranean Region.
Sci. World J. 2012:164890. doi: 10.1100/2012/164890
Ávila, S. P., Marques Da Silva, C., Schiebel, R., Cecca, F., Backeljau, T., and De Frias
Martins, A. M. (2009). How did they get here? The biogeography of the marine
molluscs of the Azores. Bull. Soc. Géol. Fr. 180, 295–307. doi: 10.2113/gssgfbull.
180.4.295
Ávila, S. P., Melo, C., Berning, B., Cordeiro, R., Landau, B., and da Silva,
C. M. (2016). Persististrombus coronatus (Mollusca: strombidae) in the
early Pliocene of Santa Maria Island (Azores: NE Atlantic): palaeoecology,
palaeoclimatology and palaeobiogeographic implications on the NE Atlantic
Molluscan Biogeographical Provinces. Palaeogeogr. Palaeoclimatol. Palaeoecol.
441, 912–923. doi: 10.1016/j.palaeo.2015.10.043
Ávila, S. P., Melo, C., Berning, B., Sá, N. B. F., Quartau, R., Rijsdijk, K. F.,
et al. (2019). Towards a “Sea-Level Sensitive” dynamic model: impact of island
ontogeny and glacio-eustasy on global patterns of marine island biogeography.
Biol. Rev. 94, 1116–1142. doi: 10.1111/brv.12492
Ávila, S. P., Melo, C., Silva, L., Ramalho, R., Quartau, R., Hipólito, A., et al. (2015a).
A review of the MIS 5e highstand deposits from Santa Maria Island (Azores, NE
Atlantic): palaeobiodiversity, palaeoecology and palaeobiogeography. Quat. Sci.
Rev. 114, 126–148. doi: 10.1016/j.quascirev.2015.02.012
Ávila, S. P., Ramalho, R., Habermann, J., Quartau, R., Kroh, A., Berning, B., et al.
(2015b). Palaeoecology, taphonomy, and preservation of a lower Pliocene shell
bed (coquina) from a volcanic oceanic Island (Santa Maria Island, Azores,
NE Atlantic Ocean). Palaeogeogr. Palaeoclimatol. Palaeoecol. 430, 57–73. doi:
10.1016/j.palaeo.2015.04.015
Azevedo, J. M. M., and Portugal Ferreira, M. R. (2006). The volcanotectonic
evolution of Flores Island, Azores (Portugal). J. Volcanol. Geoth. Res. 156,
90–102. doi: 10.1016/j.jvolgeores.2006.03.011
Baptista, L., Santos, A. M., Pilar Cabezas, M., Cordeiro, R., Melo, C., and Ávila,
S. P. (2019). Intertidal or subtidal/circalittoral species: which appeared first?
A phylogenetic approach to the evolution of non-planktotrophic species in
Atlantic Archipelagos. Mar. Biol. 166:88. doi: 10.1007/s00227-019-3536- y
Bell, B. D. (2001). Removal of rabbits from Deserta Grande Island, Madeira
Archipelago. Arquipélago Life Mar. Sci. Suppl. 2(Part B), 115–117.
Biodiversity Data Bank of the Canary Islands (2021). Government of the Canary
Islands. Available </