Are You Lichen The Food: The Tortoise Diet

Ramalina Usnea (Green) at the Centro de Crianza de Tortugas Terrestres | Jonathan Hernandez

Jonathan Hernandez

Sophomore College 2018

Professor Bill Durham

October 15, 2018

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Abstract

This paper explores the possibility of a mutualistic relationship between the lichen, R.Usnea, and the Giant tortoises throughout the Galapagos archipelago. Furthermore the paper delves into the symbiotic exchanges between the two species including water habits, vegetation supplement, and seed dispersion. Various studies from research articles and journals, ranging from studies done within the Galapagos to genus research of Ramalina outside the islands, were analyzed in order to synthesize the results. The findings demonstrate that lichen are not an adequate water source for the tortoises, but serve as a valuable food source during the their migration. The tortoise migration patterns are discussed and were analyzed along with the vegetation zones of the islands in order to support this correlation. The results shed light on the nutritional similarities between R. Usnea and the Opuntia cacti, a common food source for tortoises. In addition, the paper demonstrates the possible dispersion of lichens through tortoise movements. And lastly, this research contributes to the understanding of ecological complexity, co-interdependent studies, and paves a path for lichen to be an indicator species for the Galapagos ecosystem. Introduction

Upon landing in Baltra, immediately one might be deceived by the bareness of the land

surrounding the airport. The orange tinted lands possess such little vegetation and there might be

an iguana here or there, but this austere terrain holds more life than it makes apparent. The life

this paper discusses lives as the specks of colors adorning the rocky landscape, staining the barks

of trees, and in the highlands, endlessly hanging from branches of dense forests. The Galapagos

are widely known for their finches, iguanas, volcanoes, and especially the giant tortoises, but a

group long neglected has been the teeming system of lichen inhabiting these islands.

There are about 8300 lichen species that have been minimally recognized to have

accepted names, but more surprising is that between 50 to 80% of all Galapagos species remain

unknown. To give some context on how large the lichen population is, nearly 600 native vascular

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plant species have been reported with about 50% being endemic. In contrast, there have been 960

native species documented of which 20% could be endemic. With such a huge number and high

diversity it is evident that these organisms inhabit a vital niche in the ecosystem of the

archipelago, however their ecological importance remains unexplored. The lack of taxonomic

recognition is most likely a case of ‘taxonomy bias’; “large and iconic organisms like plants and

vertebrates have, for the most part, now been thoroughly documented, [but] the inconspicuous

ones like fungi, remain poorly known.” (Bungartz, 2016). Due to the vast amount of lichen

species present, this paper centers its focus around one specific lichen because it has been

anecdotally and photographically recorded multiple times to be interacting with the famous giant

tortoises that roam these islands. More specifically, the lichen studied in this paper is Ramalina

Usnea. The research topic of this paper came to be when I was reading Tui De Roy’s Preserving

Darwin’s Legacy and a photograph of a giant tortoise on San Cristobal with a mouthful of R.

Usnea caught my attention. The ecological interaction between these two species is useful in

order to gain a better understanding of a relationship between a flagship species and an

inconspicuous one. The implications this could hold for future studies and conservation efforts

should be valued more especially in an ever changing system that is the Galapagos.

Background

Lichen are composed of two structures: fungus and an algae or in some cases, a

cyanobacteria component. The fungus is the physical part of the lichen which takes on the

appearance of and even acts like a plant. Lichen fungi do not consume organic substrates, but

instead acquire their energy source through their algae member. Stored between their filaments,

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lichen provide space for an abundant amount of microscopic algae which supply the nutrients

that the fungus needs (Bungartz, 2016). Because of this symbiotic relationship, the fungus is

actively selecting for the best suited photobiont, a photosynthesizing organism.

Thus ultimately, this could determine which photobiont is the best fit for a particular

habitat. Mentioned earlier, there is possibility that some lichen possess a cyanobacteria structure.

These blue-green algae usually wield the ability to undergo nitrogen fixation in poorly nutrient

equipped environments. In addition to other exchanges lichen partake in, their photosynthetic

algae are a food source to microscopic snails. Other micro-mollusks then consume the smaller

snails--a microscopic food chain which could be part of a larger system (Bungartz, 2016). But

their various amount of niches does not stop there, lichen play an even more important role on

the Galapagos Islands. Throughout the archipelago, there is a scarce resource, freshwater. During

the dry season when the garua grazes over the highlands, it is the diverse forms of lichen that

capture the dense moisture. Upon condensing, the drops of water fall to the ground floor,

replenishing the cycle. With such few natural wells and seven months of little precipitation, the

island’s inhabitants are heavily helped by even this contribution. Another species who benefits

from lichen are the Darwin finches. They have been observed to often use lichen as building

material for their nests. Though it might not seem drastic since finches are opportunistic when it

comes to such matters, yet it still provides insight on the wide array of functions lichen can

perform on these islands (Bungartz, 2016).

Though many ecosystems are not explored at such small levels, the Galapagos cannot

remain in the dark about the inherently, crucial role this microcosm of diversity maintains on

these islands.

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Hypotheses

1. Tortoises turn to lichen when in need of a water supplement if freshwater availability is

low. Due to the scarcity and/or absence of freshwater on the islands of the Galapagos,

lichen (R. Usnea) can serve as a water substitute and/or source if R. Usnea has been

naturally selected for high retention of water.

2. During tortoise migration, lichen are a valuable food source. If R. Usnea proves to be

inadequate for water retention, then lichen may serve as a valuable food supply if the

usual vegetation of the tortoises’ diet is altered during their migratory periods.

3. The nutrient composition of lichen is similar to nutrients common in a tortoise diet. If the

tortoise has included lichen in its diet, then R. Usnea must share a similar nutritional

makeup like that of Opuntia echios.

4. Lichen are dispersed through the movement of tortoises by digestion. If lichen are being

consumed by the tortoises, then they are dispersed through the long movements of the

tortoises during their migratory distances.

Methods, Data, and Findings

Hypothesis I

To determine whether R. Usnea was capable of being a sufficient water supply, a study,

done by Ana Pintado et. al, was analyzed to determine the water retention capabilities of R.

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Usnea’s thalli. The morphological characteristics of R. Usnea were also analyzed along with the

drinking habits of the giant tortoises.

The morphological and anatomical structure of lichen are crucial to their ability to store

and retain water. When faced with ecological stresses, water retention capabilities are one of the

reaction mechanisms naturally selected to maintain them from drying out. For example, lichen

are known to overcome short periods of metabolic activity--when irradiance is too high that the

lichen began to dry--by morphological adaptations which improve water storage and retention

(Pintado et al., 1997).

The thalli (R. capitata) from the southern slope showed a lower dehydration rate than

those from the northern facing slope (Pintado et al., 1997). This basically means that the thalli

from the south slope held longer water retention times. In addition to water retention properties,

thalli have been shown to control evaporative resistance as well. In the Pintado et al. study, thalli

with shorter and wider (south slope) demonstrated a higher retention capacity than the thalli with

long and thin characteristics (north slope). It is also important to note that in fruticose lichen

species, the role of thalli morphology in regards to water relations are pertinently correlated,

which holds opposite for foliose lichen species. R. capitata and R. Usnea are both fruticose

species.

Figure 1. Dehydration rates of two different slope-facing thalli popul.

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Looking at R. Usnea, this lichen is morphologically characterized with (Aptroot and Bungartz,

2007):

1. Slender lobes - this signifies that the extending branch like structures are thin.

2. Pendulous thallus - the thalli are branched, threadlike, and hanging loosely.

3. Longitudinally contorted - the strands are hanging vertically, but could intertwined each

other and create a net like appearance.

R. Usnea at the Centro de Crianza de Tortugas Terrestres | Jonathan Hernandez

In contrast, the tortoises have been anecdotally noted during Porter’s expedition to be

able to retain water for long periods of time. They possess a reserve “at the root of their neck,

which contains about two gallons (Denburgh, 1914).” Not only do they have a constant storage,

but they are able to last up to a year without any type of food or water provisions. This was

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tested by the crew which overhunted the giant tortoises and left them stored away like a

provision themselves. Even more surprising, is the tortoises’ ability to reuse their bladder as an

extreme source of water. According to Darwin, tortoise-bladder water is “quite limpid, and had

only a very slightly bitter taste (Darwin, 1839).” Lastly, one of the field guides, Sabina, informed

me that she has seen tortoises drink water for long periods of time if little water is available, but

for the most part they drink and move on fairly quickly.

Revisiting the first hypothesis, there is clear evidence that the morphological

characteristics of R. Usnea make it highly unlikely for it to be an abundant source of water for

the tortoises. Because of its thin thalli, the capacity for it to have a favorable rate of water

retention is low. Thus if any case, the tortoises may simply be chewing on it for the bits of

moisture captured from the garua, but definitely nothing significant. Therefore, it is valid to say

the first hypothesis was not supported by the literature evidence and was refuted.

Hypothesis II

In order to support the second hypothesis that R. Usnea is a valuable food source during

the tortoise migration period, the vegetation zones of these islands were analyzed along with the

presence of lichen in these areas and a study done by Blake et al. which highlights the migratory

patterns of the tortoises on Santa Cruz Island.

The islands of the Galapagos typically are separated into three zones: the arid lowlands,

the transition zone, and the moist highlands zone. However, sometimes there is a fourth zone

called the uplands which comes before the highlands (Mueller-Dombois, Dieter et al. 2003), but

for this analysis three were chosen since it works best with the migratory distances study and not

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much is loss or gained with

its inclusion. The lowlands

usually contain the least

vegetation out of all the

zones. It is known as a

scrubland (Aptroot and

Bungartz, 2007) containing

other vegetation like the

Opuntia cacti and leafless

shrubs whose flowers

bloom only during the brief periods of rainfall. The transition zone is often merged with the arid

lowlands, but is higher in flora abundance. Another the demarcation is the amount of lichen

located in both sectors. In the lowlands, lichen are seen as specks or mosaics of color on the

coastal cliffs and vertical surfaces throughout the region. But as one progresses further inland

and trees become plentiful, the lichen diversity begins to be dominated by R. Usnea. In the

transition zone, Usnea is the dominant lichen instead of a variety of lichen like in the lowlands

where more of the Ramalina lichen genus make an appearance (Aptroot and Bungartz, 2007).

Ascending into the highlands, other lichen begin to make an appearance again, but Usnea is also

still found there abundantly as well. In the highlands, there the landscape is dense with Scalesia

forests and is lush in all sorts of foliage, with a year-round high consistency. Explaining the

vegetation zones are important because the Blake et. al study determined that the tortoise

migration is forage-driven therefore it is necessary to understand the vegetation in these regions.

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Coastal arid lowland vegetation | Jonathan Hernandez

R. Usnea on branch at Tortoise Breeding Center | Jonathan Hernandez

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R. Usnea on trees in Tortoise Breeding Center | Jonathan Hernandez

Looking at the migration patterns of the two areas on the island of Santa Cruz, La

Reserva and el Cerro Fatal, it is transparent that the tortoises are making a migration from the

lowlands to the highlands. The long distance movements begin in early July, as seen in figure 4.

This is due to the drastic drop in precipitation early April (figure 5). Therefore because of the

little rainfall, the vegetation quantity and quality begins to decrease. When the NDVI (figure 4)

plummets, the tortoises residing in the lowlands are affected by the lowered food supply. But to

further support the hypothesis, it is essential to note that mainly larger tortoises migrate and not

the smaller ones. This provides additional support because it highlights that the large tortoises

might be “more sensitive to declining forage quality and quantity because of their higher food

requirements. (Blake et. al).” It is evident the tortoises are in need of a foraging source, even

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throughout their migration they will need to feed for the direct energetic cost of traveling such

distances. As a consequence, tortoises may turn to uncommon forms of vegetation to supplement

their dietary needs.

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As seen on the migratory routes above, the tortoises travel through the three zones where

Usnea is known to be a dominant lichen. As the large tortoises ascend and come across the few

trees with still suitable vegetation during a dry period, it seems likely that the tortoises would

include Usnea, especially if it is excessively hanging down from the same shrubs and trees they

normally feed on. As covered earlier, lichens ability to react well to ecological stresses makes it

even more likely to be a valuable food source for the giant tortoises on their long journeys.

Therefore, during the migratory times where vegetation declines in quality and quantity, it is

supported that Usnea would become a valuable food source due to their abundance in nature.

However, this is only partially true due to one of Darwin’s encounters in the highlands. Darwin

was impressed by the fact that lichen seemed to form a “considerable portion” of the tortoise diet

in the upper damp regions of the island. This is odd due to the fact that in the highlands there is a

constant high level of greenery as seen in fig.4, so why would the tortoise still be drawn to it?

Could it be a mere choice of habit or does Usnea’s nutritional makeup share similarities to the

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tortoises’ common diet?

Hypothesis III

For this hypothesis, a study on the lichen species R. menziesii was analyzed in order to

determine its principal nutrients. Alongside this, two Opuntia cacti species were analyzed with

the same objective to compare all three food sources’ nutrient makeup. Due to the lack of studies

on Usnea, the literature chosen was on Menziesii since it is a close relative. In addition, lichen in

the same genus tend to differ in morphological features, but share extremely homogeneous

chemical makeups (Aptroot and Bungartz, 2007).

R. menziesii is a common epiphytic lichen in the woodlands of central California. Its

morphological and anatomical structures quite actually resemble those of Usnea very well, as

seen in the image to the right. The biomass from fallen Menziesii was studied to determine its

nutrient turnover to its ecosystem. Menziesii contained as much

as 32% nitrogen, 29% phosphorus, 25% potassium, 4%

Calcium, 11% Magnesium and 41% sodium (Boucher and

Nash, 1990). Its actual turnover showed extremely lower

numbers, however it still contributed a well amount to the

biomass of its habitat.

Opuntia ficus-indicus and Opuntia echios underwent a

different process in Nobel’s study to determine their nutrient

composition. The site location for O. echios was actually in the

Galapagos which contributes to relevance of the evidence. O. ficus-indicus was included mainly

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to amplify any similarities present since these nutrients are common building blocks. Listed

below are the abundance of nutrients in the sample of each cacti. (Nobel, 1983)

Fig.6. Nutrient abundance in O. echios and O. ficus-indica

When compared together, the three species share three nutrients: phosphorus, calcium, and

magnesium (figure 7). Although only the six most abundant nutrients were ranked and half of

them were shared, it is not enough evidence to support the hypothesis which could have served

as a possible answer to darwin’s highland sighting. Maybe if there was a study depicting the

abundances using the same methods would a comparison be better, but due to lack of research in

each species, this was not possible.

Fig.7. Most

essential nutrients

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Hypothesis IV

In order to support the fourth hypothesis, this paper will show the seed dispersal

capabilities of the giant tortoises on Santa Cruz island and analyze how lichens could benefit

from this.

On Santa Cruz island a study done by Blake et. al, where their team fed the tortoises a

combination of tiny colored particles in order to evaluate their digestion retention span. Another

segment of their research was to GPS track the tortoises to determine the distances at which these

particles could be spread. As seen on fig.8, the

shortest amount of time that a tortoise can takes to

digest seeds is six days, the longest being about 20

days and the average is about 12 days. Overall the

digesta period took 28 days. Looking at the next

figure, it can be assumed that around 25 days, the

tortoises can travel up to four kilometers from the

parent plant or area of seed consumption. Not only

Fig.8. Digesta retention time

that, but tortoises also disperse seeds regularly every 100 meters, meaning that they are

constantly spreading around seeds through their dung pile deposits. And since their migratory

patterns have already been discussed, it is safe to assume they are involved in the dispersal of

Usnea throughout the islands, especially with the lichen abundance in the arid and transition

zones.

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Fig.9. Distance from tagging location

According to a PhD researcher in Oregon State,

Ricardo Miranda, there is evidence showing

that lichen spores have been detected in the

dung piles of the tortoises. This is crucial

because the spores must survive the digestive

system in order to be successfully dispersed.

But ultimately, tortoises are not the only

possible mode of transportation. As mentioned

earlier, finches could possibly be the reason

why Usnea ends up hanging from tree branches. When walking through the Darwin foundation

center, there were finches pecking at the tortoises’ dung piles and perhaps this could be another

viable movement, but nonetheless still a contribution by the tortoises.

Therefore, the long digesta retention tortoises possess aid in the dispersal of seeds and

spores of many species. These large-bodied vertebrates have a dramatic role on the vegetation

dynamics of these islands due to their ability to travel long distances. Followed by the fact that

spores can survive the digestive tract, it is clearly evident that the final hypothesis is supported

and highly likely that lichen, specifically Usnea, is being dispersed through the tortoises’

movements.

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Conclusion

This report has examined four hypothesis related to the ecological interactions between

the lichen, Ramalina Usnea and the giant tortoises of the Galapagos. The first hypothesis,

predicting that this intricate relationship was water related, was not supported due to the mere

fact that the water needs of the tortoises and the water retaining characteristics of Usnea did not

go hand in hand.

The second hypothesis was partially supported. It is evident that the tortoise would turn

to Usnea as a food supplement when forage quality and quantity are declining or low, especially

during a high energy driven migration distance. However, it was partially refuted by the

anecdotal encounter of Darwin since it did not provide some sort answer as to why the lichen

was still being consumed in areas with high vegetation levels.

The third hypothesis was meant to follow up the second hypothesis, as an answer to the

partially refuted portion. However, this hypothesis was short ended mainly due to the lack of

research on this particular topic. Therefore, it did not have enough concrete information to

synthesize conclusions as to why Usnea would be a considerable portion of the tortoise diet. Yet,

it was still included because it opened up a new discussion and highlighted a section that should

be further explored.

Finally, the fourth hypothesis was completely supported. The tortoises’ ability to retain

seeds/spores for long periods of time and also travel far distances make it a suitable mode for

transportation. And since the lichen are eaten by it and some have been proven to survive the

digesta stresses, Usnea is highly likely to be dispersed through the movements of tortoises.

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As mentioned in the introduction, there is an unambiguous and undeniable importance of

this, inconspicuous yet abundant, lichen for our well loved Galapagos tortoises. Because

tortoises are so well at promoting conservation efforts, this could be a gateway for research

centering other components of their ecosystems like advancing studies on the microcosm of

lichen. The reason I advocate for this is because lichen have well been known to be indicator

species for other habitats and in the ever changing environment that is the Galapagos, having a

species which could track the health of these islands would be incredibly useful. The tortoises

have made a great population recovery, but it is still important that conservation efforts take all

precautions when dealing with an unresting archipelago. And for that, the understanding of all

ecological complexities is necessary.

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