Where did they come from and where did they Galapa-go? The fascinating story of speciation in Bulimulid land snails

Figure 1. A Bulimulid snail crawls across some lichen covering a lava rock in the humid highlands of San Cristobal.

(Author) Audrey Bennett

Bill Durham – Sophomore College: Evolution and Conservation in

Galapagos

Stanford University

14 October 2018 Abstract

Hiding under leaf piles and in small pools of moisture in the porous rocks, the small, herbivorous bulimulid snails exist almost inconspicuously from the average tourist’s eye.

However, a closer inspection into their natural history reveals an amazing story of diversification, adaptation, and evolution. This genera of snail, upon arrival to the Galapagos

Islands about 2.77 million years ago (Parent and Crespi, 2006), has since radiated into 71 different species, making it the largest adaptive radiation on the islands (Parent and Crespi,

2006). The extent of this radiation in such a small area is rivaled only by the radiation of a similar bulimulid group in Baja California (Chambers, 1991, pp. 307-325). This raises some central questions: What factors contribute to successful radiation of the the bulimulid snails? Has reproductive isolation within an island or between islands been more important for speciation?

Several hypotheses are proposed: Hypothesis 1 is that colonization event order will follow the

Progression Rule, moving from eastern to western islands. Hypothesis 2 is that island isolation and species richness are negatively correlated. Hypotheses 3, 4, and 5 are that plant diversity, an island’s elevation, and the island area are positively correlated with the species richness on that island. Data from case studies of these snails appear to support hypotheses 1, 3,

4, and 5. Lastly, this report investigates the threats that land snails face and how their adaptations to specialized environments has potentially lead to their vulnerability.

https://galapagosconservation.org.uk/wildlife/galapagos-land-snail/

Figure 2-4. Bulimulid snails occupy a variety of and have a variety of shell morphologies. (Parent)

INTRODUCTION

Natural history

The group of Galapagos includes about 71 species of land snails, all of which are endemic and distributed on most of the islands of the archipelago. (Coppois and Wells,

1987) They are also found in five of the six vegetation zones on the islands (Parent and Crespi,

2006). Adults range from 6-25 mm in length, and display a wide range of morphological traits.

This is perhaps due to the variety of microclimates they inhabit. Adults range in color from white to dull brown to dark black, often with stripes or spiral bands. The ground living species tend to be duller in color than the arboreal ones, which have paler, polished shells. There is also a large diversity in shell shape, from short and globose to long and slender (Coppois and Wells, 1987)

Potential as a study system In recent years, scientists have gained interest in these previously overlooked snails due to their amazing radiation and evolutionary history. By their very nature, islands are ideal study sites to investigate evolution, colonization, and radiation due to their isolation and simplified ecology. These snails are a particularly interesting study system since their evolutionary history is rich in speciation but very poorly understood. When lineages have diversified within islands, the clearest cases of diversification occur in taxa with low vagility on large islands with diverse habitats. This system fits that description quite well, with the islands’ distinct moisture zones providing the diversity in . This combination of factors often leads to great diversification because with their limited mobility, populations are readily genetically isolated, and the diversity in habitat creates plenty of niches for which populations can specialize. Therefore, these

Galapagos land snails are an ideal study system for radiation and speciation.

These snails have also exhibited a remarkable adaptability to a variety of habitats. A single species has radiated into species that can now survive in dry, dusty habitats as well as moist, vegetation-rich regions. They can also survive long periods of drought, which contributes to their persistence and rapid speciation. The nature of the habitats on the Galapagos contribute to the amazing radiation as well; conditions of life such as climate, vegetation, and substrate, change within very short distances, allowing for distinct species to exist in close proximity but utilize different resources (Coppois 1984).

Scientists around the world have begun to recognize the potential in this system.

Christine Parent, one of the most prominent researchers on these snails, focuses on several evolutionary questions, such as: What is the sequence of species formation? Does it match the geological sequence of island formation? Are species often formed within in an island, or do they need to colonize a new island to split definitively from a common ancestor? (Parent and Coppois, 2016). Additionally, so little is understood about this genera (their small size and elusiveness contributes to this) that scientists are still trying to answer fundamental questions about their natural history, which then inform conservation efforts.

Figure 5. Phylogenetic tree of the Bulimulid snails of the Galapagos based on combined mtDNA COI and nDNA

ITS1 sequence data. The snail outlines are roughly proportional to actual size. Species on older islands connect at deeper nodes. Numbers above branches are Bayesian posterior probabilities. (Parent, Caccone, and Petren, 2008)

Adaptive radiation

Before delving into hypotheses, a strong understanding of adaptive radiation will be useful in understanding the mystery of the high species richness. Adaptive radiation is defined as the differentiation of a single ancestor into an array of species that inhabit a variety of environments and differ in morphological and physiological traits to exploit those environments

(Schluter). The mechanism is as follows: more ecological niches, whether that be habitat type or food source, allows for more specialization, which given enough time can lead to reproductive isolation and isolation. Thus, phenotypic differences between populations originate from differences in environments they inhabit and resources they consume. These differences subject the species to unique selection pressures, which drives unique adaptations to that ecological niche. In addition, competition can drive co-occurring populations to exploit new resources and environments (Schluter). For example, competition for habitat space could drive a subset of a snail population in a region to move to a more arboreal habitat.

This also suggests that rates of such divergence are dependent on the number of niches available, which could be a partial explanation to the snails’ incredible species richness. Given the high barrier to entry, islands as isolated as the Galapagos have a wealth of different resource types underutilized by different taxa, providing a great opportunity for divergence (Schluter).

Therefore, ecological opportunity is largely dependent on timing; a species colonizing a remote archipelago or surviving a mass extinction is in a powerful position to speciate, given the number of available ecological niches.

This paper will investigate the mechanisms of this impressive example of radiation to better understand the factors that influence species richness on islands. Island biogeographical theory says that species richness is dependent on three main rates: colonization, speciation, and extinction (Parent and Crespi, 2006). My hypotheses will focus on the dynamics of these three rates, which will in turn contribute to the overall understanding of how such a high number of species has remained distinct in a relatively small land area (7880 km2) (worldatlas.com).

Figure 6. Species richness on an island is affected by colonization, speciation, and extinction rates. The three main influences of these factors are listed above them. This paper will investigate colonization, speciation, and extinction of the snails and how it affects species richness.

COLONIZATION

The initial colonization event, their “lucky break” that allowed such speciation, is thus a key part of the snails’ evolutionary history. However, mechanisms of dispersal and the exact common ancestor is still surprisingly unknown. Parent, Caccone, and Petren (2006) found that there was one single colonization event from the mainland, while other genera of snails on the

Galapagos like Bapstinus have about three. They hypothesize that the Galapagos bulimulids are closely related to the continental South American bulimulids due to morphological affinities.

However, this has not been genetically confirmed, and extinctions and range shifts often makes identifying the initial colonizer difficult to confirm. The time of the initial divergence from their closest relatives is also unknown, since there is not a reliable molecular clock for this taxonomic group.

Dispersal mechanisms

The bulimulid snails have certain adaptations that could have aided in their survival across the 1000+ km of ocean. They can close their operculum to prevent moisture loss, and can go into a state of aestivation, which is a state of dormancy and lowered metabolic rate to cope with arid conditions. One hypothesized mechanism has been travel via birds. Rafting on vegetation, though originally proposed, seems less likely since on certain islands, there are no snails in the lower elevation zones and only found in the moister, high elevation zones. These snails have also never been found in the littoral zone, which is the one closest to the shore.

After examining land snails across a variety of islands in the Pacific, Vagvolgyi (1976) argues that the most convincing mechanism of dispersal is wind. He noticed that while 27% of the land snails on the mainlands surrounding the Pacific are deemed minute (less than 100mm),

60% of snails that inhabit the islands in the Pacific are minute. Aerial dispersal is the primary mechanism that provides an advantage for a smaller body size.

Progression Rule

Colonization can be broken up into two types: the initial colonization event from the mainland, and the subsequent inter-island colonizations that allowed this genus to spread throughout the archipelago. My first hypothesis focuses on the combination of these two types of colonization. I hypothesize that the colonization event order will follow the Progression Rule, moving from eastern to western islands. The reasoning behind this hypothesis lies in one of the most powerful ecological forces of the islands: the currents. Panama and Humbold Current run along the coasts, perhaps gathering rafting along the way, till they join at the equator and move westward in the South Equatorial Current. The wind patterns also follow a similar pattern.

This movement westward could contribute to an initial colonization event on the easternmost island, and subsequent inter-island colonization events moving westward. Also, the Progression

Rule is more pertinent for less vagile organisms, which are subject to the forces of the currents and winds for dispersal more so than birds, for example.

Figure 7. Schematic of proposed colonization sequence. Española is hypothesized to be the first island colonized by the mainland ancestor. The arrows represent colonization events within the Galapagos. The pattern seems to generally follow the order of geological formation.

A study by Parent and Crespi (2006) supports this hypothesis. Based on molecular phylogenetics, the phylogeny obtained supports the progression rule in that the older, easternmost islands support the species that connect at deeper nodes on the phylogenetic tree.

The proposed colonization sequence begins at Española, one of the oldest islands in the archipelago, and moves westward. Thus, the colonization sequence roughly parallels the geological formation of the islands.

Island isolation

My second hypothesis on colonization is that island isolation and species richness are negatively correlated. I hypothesized that increased isolation would decrease chance for inter- island colonization, thus decreasing the species richness. Work done by Parent and Crespi (2006) revealed that this relationship is more nuanced; they found that insularity is a significant predictor of species richness resulting from interisland colonization alone, as I hypothesized. However, when they considered overall bulimulid species richness, and not just species richness as a result of colonization, they found that island insularity has no effect on overall bulimulid species richness. Further study shows that for all but two island species assemblages, there has only been one or two colonization events, which indicates that within-island speciation has had a significantly more important role in the formation of new species. Therefore, the mechanism needs to be considered when understanding the factors that affect speciation.

Figure 8. The y-axis is log(species richness of bulimulid species per island +1). Regression of the number of bulimulid land snail species on the Galapagos island corrected for island age against island insularity measured as the distance to the nearest major island. (Parent and Crespi, 2006)

The degree of isolation from other islands in the archipelago affects the number of colonization events on that island. The study by Parent, Caccone, and Petren (2008) found that polyphetic assemblages were found on islands more centrally located in space and time, like

Isabela, Santa Cruz, Pinzón, and Santiago. This means that the populations on these central islands probably experienced more frequent inter-island colonization, while more isolated islands like Española, San Cristobal, and Floreana are occupied by monophyletic assemblages that have since speciated. Wolf and Darwin, despite their large size and promising habitat diversity, have no record of land snail fauna, perhaps due to their isolation (Parent and Crespi, 2006). Thus, island isolation affects frequency of inter-island colonization, which has little to no impact on overall species richness. Future studies could investigate if the area of coastline affects frequency of colonization, which would suggest that dispersal occurs through rafting on vegetation.

Figure 9. A snail traverses a lava rock in San Cristobal. (Author)

Figure 10. A group of Bulimulis nux cluster on a fallen tree. (Parent, Arkive.org)

SPECIATION

The isolation of the Galapagos may act as a barrier to dispersal and colonization, but it simultaneously acts as a mechanism of speciation. The isolation of these archipelagos (especially given the snails’ low vagility) mean that reproductive isolation occurs more readily.

As Parent and Crespi’s work (2006) suggests, perhaps the more important mechanism affecting species richness is speciation upon arrival. Thus, we now shift focus from the frequency and mechanisms of arriving on the island to what happens to a population upon arrival. Schluter (2000) writes that there is a tendency of species to become more specialized as competition drives populations to utilize different available resources. As populations begin to make use of different resources, each new environment subjects the species to unique selection pressures that establish different fitness valleys and peaks. Competition drives species to exploit new resources and environments when they become subject to selection pressures, and natural selection pressures favors this divergence to reduce competition for resources. Rates of divergence are also dependent on biogeographical and ecological attributes of the island, which will be the focus of my hypotheses on this topic.

Environmental heterogeneity

My hypotheses are grounded in the work done by Stein, Gerstner, and Keft (2014), which is a meta-analysis that compiles studies done on the effect of environmental heterogeneity on species richness (not bulimulid snail specific). They write that heterogeneity creates new niche spaces, refuges to increase species persistence, and opportunities for isolation, which lead to divergent adaptations. This study found that heterogeneity in both biotic conditions (land cover, vegetation) and abiotic conditions (climate, soil, and topography) increased species richness.

Figure 10. Mean effect size for different measures of environmental heterogeneity (EH) and for biotic vs. abiotic EH.

Lines show 95% confidence intervals. Letters indicate significant differences among EH subject areas. (Stein, 2014)

The next logical question is, how do we measure environmental heterogeneity? Stein

(2014) looks at the number of plant species, the diversity of land cover types, the elevation range, the heterogeneity in soil composition, and microtopographic structures as measures of heterogeneity. I chose plant diversity and elevation as the measures of heterogeneity of concern for this system. Snails use plants as food sources and habitat, and plant diversity is especially important for specialized herbivore species richness. The habitats on a given island are very elevation-dependent due to varying levels of moisture availability, so I hypothesize that an island that reaches a greater elevation will have more habitat niches. My last hypothesis is that island area and species richness will be positively correlated. Although area is not necessarily correlated with environmental heterogeneity (it is easy to imagine a large, homogenous forest), larger island area will mean more resources are available, and thus the island can sustain larger populations. Large populations mean better chance of survival, which is an important part of speciation; the new species must be strong enough to persist. Additionally, larger area will provide more room for reproductive isolation; achieving reproductive isolation on a small island seems more difficult.

As a side note, some people hypothesize that the relationship between environmental heterogeneity and species richness might be more hump-shaped rather than strictly positive since too much heterogeneity on an island might reduce a particular species’ habitat area. This extent of the relationship between heterogeneity and species richness was not investigated in Stein 2014 nor in my paper.

Figure 11. Profile of transect from Cerro Puntudo. The presence of bulimulid species is indicated by ______

(abundant or common), ------(present), and ****** (extinct species. Main characteristics of vegetation and substrate are on the bottom. (Coppois 1984)

Figure 12. Habitat zones in the Galapagos along an elevation gradient. (Galpagos ecosystems, web.mit.edu)

Habitat distributions It is first beneficial to understand species distributions across an altitude and habitat gradient. Coppois (1984) found that distributions on Santa Cruz Island of species are related to the climatic gradient (which is indicated by plant zonation) and the nature of substratum. He found a more distinct zonation near the summit zone on the northern slope, and in the south, areas of neighboring species are more overlapped. The habitat zones of the islands are typically divided into seven vegetation zones: the pampa zone, the miconia zone, brown zone, scalesia zone, transition zone, arid zone, and coastal zone, each with distinct plants, soil acidity, and moisture levels. Coppois noted that each species have very tight zones, with ranges sometimes as small as 100m (along a transect running from the peak to the base of the island). Some species appeared to be highly specialized while others have wide distributions. The ochsneri has a wide distribution, and can live in forest litter, or hide in small cavities under fallen logs, roots or rhizomes. It has also been seen on the vegetation of the herb and shrub zone. Bulimulus blombergi also has a wide distribution. (Coppois and Wells, 1987). The Bulimulus cavagnaroi is restricted a very narrow band, 300m wide. Taxon 23 was found under blocks of lava, which is a usual hiding place for an arid zone snail. The Bulimulus tanneri was the only species found alive and in abundance along this transect in the arid zone, hiding in cavities under blocks of lava, aestivating. When more than one species was found in the same area, they seem to partition it by either living in the open, or on tree trunks and vegetation, or on rocks. Some even specialize the type of plant they live on (Parent and Crespi, 2006). Thus, conditions of each species are determined by altitude, local climate, vegetation, and substrate, which change within very short distances. This system is a unique opportunity to study the limiting factors of habitat corresponding to each species.

Plant diversity A study by Parent and Crespi (2006) found that species richness of the bulimulids was strongly positively correlated (p<0.001) with habitat diversity (measured as the number of plant species), which supports my hypothesis. Plant diversity is an indicator of the diversity of microclimates and the number of ecological niches that can support different species.

Figure 13. The y-axis is log(species richness of bulimulid species per island +1). Regression of the number of bulimulid land snail species on the Galapagos island corrected for island age against habitat diversity measured as the number of plant species. (Parent and Crespi, 2006)

Island elevation

The same paper (Parent and Crespi, 2006) also found that species richness and island elevation were positively correlated. This supports my hypothesis. Vegetation zones are dependent on humidity levels, which vary with changes in elevation. Thus, an island that reaches a greater elevation will have more humidity levels and vegetation zones, creating more ecological niches. For example, there are 18 species on Floreana, 15 on San Cristobal, and 24 or 25 on Santa Cruz. The high island of Pinta with only one species is an exception, but it is also very isolated (Coppois and Wells, 1987).

Figure 14. The y-axis is log(species richness of bulimulid species per island +1). Regression of the number of bulimulid land snail species on the Galapagos island corrected for island age against island elevation. (Parent and

Crespi, 2006)

Coppois and Glowacki (1983) have found certain traits that correlate with elevation levels. There is a significant positive correlation between the degree of shell roundness and elevation. Shells that are rounder maximize the shell surface area to allowed body area ratio, however rounder shells have larger openings, which allow for more moisture loss. Thus, snails have adapted to have skinner shells at lower elevation levels, perhaps in response to lower moisture levels.

Figure 15. The x axis is the distance from the highest point of the island, thus as x increases the elevation and moisture levels decrease. The changes in shell morphology are represented pictorially. (Coppois 1984)

Figure 16. X-ray image of a bulimulid shell. X-ray imaging was used by researchers to further understand the relationship between shell morphology and habitat. Taller spires and smaller apertures are prevalent in arid coastal areas, while wide-bodied shells are common in humid highlands. Island area

My final hypothesis was also supported. Parent and Crespi (2006) found that species richness and island are positively correlated as well. Perhaps larger islands are able to support larger populations. Larger island area is also conducive to retaining reproductive isolation.

Figure 17. The y-axis is log(species richness of bulimulid species per island +1). Regression of the number of bulimulid land snail species on the Galapagos island corrected for island age against island area. (Parent and Crespi,

2006)

Complexity

My hypotheses have investigated the influences of geography (island area, elevation, insularity) and ecology (habitat diversity) on colonization and speciation among bulimulid snails.

These different factors interact as well; for example, island insularity decreases the rates of colonization of plants, potentially decreasing the habitat diversity on that island. It is incomplete to think of this system without considering time scales; new islands have yet to become saturated in the number of species they can support, and older islands seem to harbor more species. For example, young islands like Fernandina and Isabela have fewer land snail species than expected based on their area, elevation, and insularity (Parent, Caccone, and Petren, 2008). As islands age, they begin to sink, thus decreasing in elevation (and perhaps the number of species they can support). Older islands also have more time for species to go extinct. Cyclical patterns in climate, like ENSO events, could also affect vegetation, which indirectly affects the snails. The factor of time demonstrates that species diversity equilibrium is dynamic and changes through time

(Parent, Caccone, Petren, 2008).

Figure 18. The relationship between colonization, speciation, and extinction and the factors that influence them are much more complicated and interconnected that the previous model in Figure 6.

EXTINCTION

Threats

Although many species have evolved effective adaptations to the arid zones, drought still has a significant effect on these snails. has been extinct since the end of the last century, and the drought has had a noticeable impact on many species inhabiting the Santa

Cruz highlands. Live snails have rarely been found north of Cerro Puntudo since then.

El Niño, which brings heavy rainfall to the islands, benefitted the lower arid regions. In normal conditions, the Scalesia pendunculata forms a canopy 5-10m off the ground level, providing permanent shade and humidity. However, the scalesia forest in the highlands began to rot during the excessive rainfall, and when the trees fell it exposed the herb and shrub layers. The subsequent hot years meant that many populations suffered from sun exposure. It takes at least a decade for the forest to return to its previous form (Coppois and Wells, 1984).

Climate change has the potential to increase the intensity of El Niños in the future, thus impacting highland snail populations. Additional human-driven threats include the destruction of habitat, especially on Santa Cruz Island, for farmland. On Floreana, people have cleared plants to create pastures for cattle and horses. The invasive Wasmannia auropunctata, a fire ant, preys on the juveniles and eggs. In areas of high ant density, the bulimulid populations are low or even absent with only empty shells remaining. There has been few observations of direct attacks, but snails often withdraw into their shells in the presence of these ants. Additionally, snails often lay their eggs in empty shells, which are also used as nests by these ants (Coppois and Wells, 1987).

Other threats include the black rat Rattus rattus, which typically preys on the larger snail species. The snail populations at El Junco on San Cristobal has been decimated, and signs of rat predation have been found on Santa Cruz, Santiago, and Floreana (typical signs are empty shells with rat bite marks). Introduced goats have decimated vegetation, especially the Scalesia forests, on at least nine islands. Exotic plant introduction impacts the local vegetation, which in turn impacts the snails. Psidium guajava trees have been introduced at Cristobal and Floreana, where now only empty shells are found (Coppois and Wells, 1987). Thus, many of the anthropogenic impacts on local vegetation have direct effects on the local snail populations as well.

Figure 19. A bulimulid snail on the back of a tortoise, San Cristobal. (Author)

Conservation

More than 30 endemic bulimulid snails are now considered endangered. Despite these pressing threats, current conservation plans do not take snail populations into consideration. For example, many of these threatened species live in the 10% of the Galapagos that does not have national park status (Coppois and Wells, 1987). Additionally, a road to improve access to the airport across Santa Cruz collected gravel from Cerro Maternidad, the locality of B. cavagnaroi.

Their range has thus been dramatically reduced, and a gravel pit on the slope may alter the microclimate for the remaining population. This exemplifies the danger of specialization; anthropogenic shifts to the environment can turn a specialized adaptation into a vulnerability.

Ideally, future conservation efforts will prioritize removing invasive species and protecting the remaining habitats while also funding research to better understand their ecology and natural history.

These relationships emphasize the importance of investigating the situation as a social- ecological system. Ignoring the relationships humans have with the resources that snails also depend on would be incomplete. Additionally, the local economy, politics, and needs of local peoples affect their relationship with the natural resources. Conservation efforts in the future will need to consider the needs of both the ecosystem and the social system to work towards a solution.

Figure 20. A Sophomore College student investigates an empty shell found in the San Cristobal highlands. (Author)

Figure 21. The social-ecological system, which incorporates humans and their needs and influences into the system.

Adapted from Dr. Bill Durham.

Figure 22 and 23. Bulimulid snails with different shell textures and colors. (Parent, Arkive.org)

CONCLUSION

This report has explored the applications of evolutionary theory to the Galapagos

Bulimulid land snail species. Within the framework of island biogeography theory, which says that species richness is affected by colonization rates, speciation rates, and extinction rates, we investigated the factors that contribute to these rates. Research supported my first hypothesis that colonization followed the Progression Rule. However, research refuted my second hypothesis, which was that species richness would be negatively correlated with an islands’ isolation. This supported the idea that colonization rates are less important for species richness in this case.

When considering the factors that affect speciation rates, my hypotheses were supported in that plant diversity, island elevation, and island area are positively correlated with species richness on a given island. These factors increase environmental heterogeneity and opportunities for reproductive isolation and ecological specialization. Moreover, this paper demonstrates that biogeography and ecology are key predictors of how many species are present on an island, we must consider the processes of diversification (colonization or speciation upon arrival) when trying to understand the factors that promote . Despite understanding these trends, speciation and the ability of an island to support unique species is driven by so many other factors that are interrelated, like island age, human presence on the island, and competition with other genera of snails or small herbivores for habitat, that an effective model is much more complex than the one I have constructed in figure 6.

Lastly, these snails face many anthropogenic threats, and 40% of the bulimulids are threatened. However, current conservation efforts do not seem to take their needs into account, and the question of how to get the public to care about such a small, inconspious snail is only growing in importance. While some may question how we can justify allocating funds for their protection, I would argue that their beauty, ecological role, and amazing evolutionary history mean that we have a lot to learn from these small snails.

This paper was peer-editted by Sammy Price and Shannon Yan.

Bibliography

Chambers, S.M. 1986. ‘2 new bulimulid land snail species from Isla-Santa-Cruz, Galapagos-

Islands. Veliger 28:287-293.

Coppois, G. (1984) ‘Distribution of bulimulid land snails on the northern slope of Santa Cruz

Island, Galapagos.’ Biological Journal of the Linnean Society, 21: 217-227.

Coppois, G., Wells, S. (1987) ‘Threatened Galapagos snails.’ Oryx, Vol. 21, Issue 4, pp. 236-

241.

Galapagos Ecosystems [online]. Available at

http://web.mit.edu/12.000/www/m2008/teams/egilbert/ecosystems.html (Accessed 8

September 2018)

Galapagos Islands, World Atlas [online]. Available at:

https://www.worldatlas.com/webimage/countrys/samerica/galapagosislands/galaplandst.h

tm (Accessed 13 October 2018).

Parent, C. Bulimulid snail. [online]. Available at:

https://galapagosconservation.org.uk/wildlife/galapagos-land-snail/ (Accessed 10

September 2018)

Parent, Coppois. (2016). ‘Bulimulid land snails’ in de Roy, T., (ed.) Galapagos: Preserving

Darwin’s Legacy. 2nd edn. New York: Blomsbury Natural History.

Parent, C. E., Caccone, A., Petren, K. (2008) ‘Colonization and diversification of Galapagos

terrestrial fauna: a phylogenetic and biogeographical synthesis.’ The Royal Society, Vol.

363, Issue 1508.

Parent, C.E., Miguel, S.E., Coppois, G. (2016) ‘CDF Checklist of Galapagos terrestrial and brackish water snails.’ CDF.

Parent, C. Galapagos land snail [online]. Available at:

https://www.arkive.org/galapagos-land-snail/bulimulus-nux/ (Accessed 13 September

2018)

Parent C.E, Crespi B.J. (2006) ‘Sequential colonization and diversification of Galápagos

endemic land snail genus Bulimulus (, ).’

Evolution, 60:2311–2328.

Schluter, D. (2000) The Ecology of Adaptive Radiation. 1st edn. New York: Oxford University

Press Inc.

Stein, A., Gerstner, K., Kreft, H. (2014) ‘Environmental heterogeneity as a universal diver of

species richenss across taxa, biomes and spatial scales.’ Ecology Letters, 17: 866-880.

Wager, Funk. (1995) ‘Hawaiian Biogeography.’ AGRIS.