Functional Interpretations of Chemotaxis in Migrating Organisms

Table of Contents

Abstract

There are many functional applications of chemotaxis that form the stepping stones of animal migration. Investigating trophic chains – dynamic networks of interacting species – reveals how migration and changes in population density shift environmental conditions of an ecosystem. It was shown how fish and algae populations can reduce extinction within a region and increase the abundancies of populations. Conversely, food chains also affect migrating animals, as this was shown for various species using isotropic maps. Diadromy is the fascinating life transition of some fish from fresh water to sea water. Many physiological and chemical adaptations occur during this stage, most notably the remodeling of osmoregulation. Diadromy in Anguilla eels is investigated; it was found that juveniles undergoing the metamorphosis earlier had a tendency to migrate at an earlier stage. In salmon, secretion of sexual hormones, like testosterone and estradiol amongst others, favor upstream migration and disfavor downstream migration. These hormones can also inhibit smoltificaiton in salmon. The brown planthopper, a rice-feeding pest, uses gene expression as an adaptation to the oogenesis-flight syndrome, which prevents migration and reproduction to occur in the same life cycle.

Introduction

Migration involves movements of animals at a large scale, either by the animal travelling a vast distance or an environment encountering a drastic shift in its flora and fauna as a population relocates for a time.  This creates a duality between approaches in understanding how migration affects biological systems, as researchers can take an organism- focused approach or an environment- specific approach. Central to this is the concept of chemotaxis – the movement of an organism in response to chemical stimulus.

The trophic changes of an environment can be used as an information source for migration. Subtle environmental changes can have drastic impacts on smaller organisms at the bottom of a trophic chain, which can then create feedback loops to signal migration. Likewise, microscopic organisms can considerably change the chemical makeup of their environment through their metabolic processes, and therefore their migration can be life-altering for the other members of their ecosystem. The inverse perspective, looking at the trophic chain’s effect on an organism such as through stable isotopes, can be a very useful tool in understanding the aspects of its journey.

Migration is just as much a lifestyle change as it is a change in location, and as a result there are many adaptations it must go through to match its new surroundings and routine. Signals such as the salinity of an eel’s surroundings can trigger the hormonal change necessary to facilitate lifestyle adaptions.

The motivations for a species to migrate are also integral to its chemical activity and how it responds to its environment. An example of this is salmon, which interrelates its migration with its reproductive cycle. It is the sexual hormone which signal migration, and salmon go through further hormone changes to switch from freshwater to saltwater.


Trophic Chains

As animals migrate, they pass the boundaries of their food web and traverse the food webs that lie along their migratory route. The food chain, or trophic chain, is made up of many interwoven food chains to create a representation of feeding relationships within that ecological region. These dynamics can be interpreted as the networks of more specific, local food webs connected by the movement of its species (Mougi, 2021). Animal migration, either seasonal or reproductive, supports food webs by reducing extinction within a region and increasing the abundancies of populations (Mougi, 2021).

Fig. 1 Food chain example, desert grassland [adapted from Cain et al, 2008]

There are two interesting ways migration interacts with food chains; through population dynamics, which when applied to the scale of microorganisms affects environmental chemistry, and in the concentration of isotopes, which can be used to determine the details of a migration event. 

Environmental chemistry

The displacement of species from certain habitats can alter the ecosystem around them. This can be directly seen by the interactions of migratory marine animals and the microscopic organisms that live lower on the trophic chain. In a six-year study done by Broderson et al., it was found that the proportion of fish migrating was directly related to the mean size of zooplankton in the lake, plankton increasing with fish being away. While fish population was positively related to lake temperature, zoo- and phyto- plankton population was found to be independent (Broderson et al., 2011). It was instead related to the number of fish being away from the lake, as there is less predation on the plankton (Broderson et al., 2011).  The plankton go on to affect the chemical composition of the water by the rate at which it undergoes photosynthesis.

Fig. 2 The relationship between phytoplankton, zooplankton, fish migration, and temperature. (1) spring return migration, (2) zooplankton migration, (3) phytoplankton spring phenology, (4) Zooplankton spring phenology, (5) phytoplankton phenology, (6) Zooplankton phenology [Adapted from Broderson et al., 2011]

Going even further down the food chain bring us to algae, which can drastically shift the environmental conditions of an ecosystem through its migration and population density. Algal blooms, such at the red tide, result from the migration of harmful algae that migrate toward the surface (a phenomenon called diurnal vertical migration). The conditions that allow these toxic phytoflagellates to flourish, studied by Shikata et al., 2015, are an interplay of nutrient availability and photosynthesis. Spectrophotometry was used to understand the migration cycle of four algae species, particularly in the context of light wavelength.

Isotropic maps of migration

In the inverse scenario, we can look to the effect of the food chain on the migrating animal to gather a more fulsome picture of its route. This is done through the analysis of stable isotopes, which are variations of the same atom that exist in quantities specific to a certain region or time. Tissues like hair, feathers, or nails – made of keratin – are metabolically inert after they have been synthesized, so they create a fixed location on the isotropic record based on where the tissue was synthesized (Hobson et al,. 1999). Marine food chains tend to have more isotopes, particularly 13C, 15N, and 34S (Hobson et al., 1999).

Stable isotopes allowed van der Merwe et al to couple conservation efforts of the African elephant, Loxodonta africana, with migration studies. The ratios of different isotopes were measured to reflect different aspects of its environment; 13C and 12C were measured in elephant bone collagen and then converted to carbon dioxide and nitrogen, reflecting the mixture of foliage and grasses in its diet; 14N and 15N were measured to show the change in rainfall; 87Sr and 86Sr were measured to show the geology of its locations (van der Merwe et al, 1990).

Fig. 3 Morphology of elephant tusks used to determine where to draw isotope samples from [adapted from ivoryid.org]

In bird migration, deuterium can be used a geographic marker, alongside the isotopes used in land mammals (carbon reflecting vegetarian diet, nitrogen reflecting water data and strontium reflecting geology) (Kelly et al, 1998). The deuterium is taken from feathers, as it needs to be taken from tissue that was renewed seasonally, making feathers the best option for sampling. Deuterium reflects the latitudinal pattern of rainfall in the growing season of plants, completing the picture needed to map the migratory route.

Fig. 4 Patterns created by contours of deuterium variances in rainfall in North American growing season [adapted from Hobson et al, 1999]

Lifestyle transition and migration

The Anguilla Eel

Life transition is highly linked to migration patterns of animals. To better understand these phenomena let us take an example on aquatic animals that migrate between fresh and saline water. This phenomenon is what is called Diadromy. Diadromy is a term that qualifies animals that migrate between fresh and saline water, these migrations are for most a regular physiological phenomenon that occurs for most members of the species and is obligatory. This phenomenon is very pertinent in the context of our paper, since as there switching between environment, these fishes undergo a variety of physiological changes both on the hormonal and osmoregulatory level. We will explore such phenomenon by looking at the fascinating metamorphosis that the eel undergoes while transitioning from a fresh, to a saline water lifestyle.

The Anguilla eel is a migratory eel that migrate 5000 km across the Atlantic twice during their life span. They first hatch in saline sea water, then they move with the Gulf stream for over 500 kilometer till they reach Europe. Once there, they metamorphose into what we call glass eel before migrating till they reach the estuaries where they metamorphose once more into a pigmented form called “elvers” , they then start to move towards fresh water where they will grow into adult yellow eels. Then after a few years those eels are going to migrate again towards saline water and metamorphosis again into their final form the silver eel. The lifecycle of this amazing creature can be seen in more detail in figure 5.

 Fig. 5 “Life history of the European eel (Anguilla Anguilla) “ [Adapted from A. Cresci et al, (2020)   ” Glass eels (Anguilla Anguilla) imprint the magnetic direction of tidal currents from their juvenile estuaries.”]

We can then hypothesis on the timing of the metamorphosis and link it to the animal “life transition “from a stationary to a migratory state and from a freshwater to a saline transition. To test our hypothesis, we can refer to the research conducted by Minamidai Nakano from the university of Tokyo, in his paper “Metamorphosis and inshore migration of tropical eels Anguilla spp. in the Indo-Pacific” he refers to this relationship between life transition and metamorphosis. To do so they extracted and compared different Otolith from different sample of eels. (Refer to figure 6 for more information about otolith).

 Fig. 6 Picture of an eel otolith adapted from Jellyman et al. (2006)

The otolith is a calcium carbonate structure of the inner ear and it’s the most used structure for determining the age of fish including eels. These structures grow over the lifespan of the fish and accumulate material on its outer surface. Similarly, to tree trunk we can determine the age of a specimen by counting those circulars like structure around the nucleus as shown in the figure.

By comparing the otolith width from the edge at different ages of the eel’s life one can interpret the phases and divide them into 4 distinct phases. Phases I and II represented preleptotene state and leptocephalus phase, whereas phase III metamorphosis and phase 4 glass eel. Now if we look at the relationship between the timing of the metamorphosis and the recruitment to freshwater, we can clearly see a high correlation between the two. In fact, the juveniles undergoing the metamorphosis earlier also had a tendency to migrate at an early stage. Furthermore if we graph the age of recruitment in function of the age metamorphoses of several specimen, we can clearly see that the two are almost proportional, as shown in figure 7.

Fig. 7 Relationship between the age of recruitment and the age of metamorphosis of the eel [ adapted by Minamidai. Nakano and all. from Metamorphosis and inshore migration of tropical eels Anguilla]

This information confirms are initial hypothesis linking the metamorphosis of eel too the migration from Fresh to saline water. But one might ask themselves the changes in metabolism related to that metamorphosis. In other words, how do eels adapt from living in fresh water environment to a saline one. One very important factor to take in consideration when switching from an environment to another is the maintenance of plasma osmotic regulation. To put it simply, sea water is hypertonic to fish which means that there’s is a higher concentration of water inside the fish than outside the fish. Which results in the water being continuously lost through the skin of the fish. As a result, sea water creature’s intake a lot more water, while filtering out the salts through there kidney and gills. On the other hand, freshwater creatures have the inverse mechanism, since this time water is hypotonic to them, they urinate more frequently in order to maintain osmotic equilibrium. This leads us to question how eels are able to survive in both saline and freshwater environment, if the mechanisms for each are very distinct from one another.

Fig. 8 Picture of glass eels [Adapted from “Glass eels (Anguilla anguilla) imprint the magnetic direction of tidal currents from their juvenile estuaries” by Alessandro Cresci]

The answer to this question lies in the ability of the eel’s body to adapt accordingly to the environment it is in. When the eel enters saline water, there body start producing concentrated NACL urine as well as enzyme that exude salt through there skin, hence rendering water hypertonic to them and allowing them to intake it into there body. Similarly, when switching to fresh water, the eel produces another enzyme that pushes salt back into there body and dilutes their urine. These mechanisms make the eel extremely versatile and able to transition very easily between lifestyles during there long migrations!

Migration and Reproduction

Control of Salmon Migration by Sexual Hormones and Smoltification

Fig. 9 Salmon in air during upstream migration. [Adapted by https://www.pxfuel.com/en/free-photo-oiumm]

Salmon must migrate hundreds of kilometers each year for reproductive purposes and to complete their life cycle. They have a very challenging task and use various tools and techniques to achieve this great feat, such as magnetoreception, olfaction, photoreception, and optimal jumping. However, these sensory and behavioral adaptations do not tell them when to migrate, and in which direction (upstream vs downstream). Downstream migration is the act of travelling from the spawning area of fish – generally a river – to the sea, whereas upstream migration is the opposite action. In fact, this seasonal information is transmitted to salmon through their sexual hormones. Research has shown that it is their level of sexual hormonal secretion that will dictate whether the salmon will migrate or not for a particular year.

The research performed by Munakata et al. (2000) demonstrates that testosterone (T), estradiol-17beta (E2), 11-ketotestosterone (11-KT), and 17α,20β-dihydroxy-4-pregnene-3-one (DHP) were the sexual hormones to control migration. In figure 10 below, a control group of juvenile salmon (no sexual hormones at this stage) and 5 experimental groups of juvenile salmon administered with either T, E2, 11-KT or DHP hormones were investigated to measure the percentage of migrating and non-migrating fish. It was observed that all salmon from the control group travelled downstream, whereas, with the experimental groups, this rate was decreased. For figure 11, upstream migration was evaluated for adult salmon. They were castrated to not naturally produce sexual hormones and the experiment was repeated. The experimental groups showed a higher rate of upstream migrants than the control group. Although the effects of these hormones did not always show consistent results, it was generally concluded that their secretion in salmon encouraged upstream migration while equally discouraging downstream migration (Munakata et al., 2000).

The reasons are for this behavior are obvious: there is no purpose of the salmon to return home if they are not ready for reproduction. Their return would be in vain. Conversely, if a salmon does not yet show the signs of sexual maturity, it can travel downstream to reach the ocean and perform its seasonal migration. The practicality of the mechanism is quite innovative because it shows that salmon don’t simply rely on seasonal changes to control their migration. Instead, salmon have chemically adapted to maximize their reproductive success. In fact, it was found that males that mature early and show early signs of sexual hormone secretion do not travel downstream in spring (Munakata et al., 2000). If they were to do so, their chance of survival upon return would be extremely low. Instead, they wait until autumn, their spawning season, and migrate upstream to reproduce.

Fig. 10 Percentage of downstream migrating and non-migrating salmon (1st row) and levels of sexual hormones (T, E2, 11-KT, DHP) and thyroids (T3, T4) for a control group of salmon and 5 experimental groups of salmon with infused hormones. [Adapted by Munakata et al., 2000]

Fig. 11 Percentage of upstream migrating and non-migrating salmon (1st row) and levels of sexual hormones (T, E2, 11-KT, DHP) and thyroids (T3, T4) for a control group of castrated salmon and 5 experimental groups of castrated salmon with infused hormones (T, E2, 11-KT, DHP). [Adapted by Munakata et al., 2000]

Fig. 12 “Morphological differences between Atlantic salmon parr (top) and smolt reared in the wild.” [Adapted by McCormick, 2013]

Salmon must also perform another chemically fascinating transition before downstream migration: smolting. This is the equivalent to diadromy, but for salmon. As stated above, the fish must undergo many changes – physiological as well as metabolic – like changing the size and color of its limbs and adapting its osmoregulation metabolic process to withstand saline sea water. Regulation of smoltification is controlled by many factors, such as temperature, light, and thyroid hormones (McCormick, 2013). But most interestingly, its regulation has also been associated to sexual hormones (Ikuta et al., 1987). High secretion of testosterone was found to inhibit smelting, which prevents juvenile salmon from reaching the sea entirely (Ikuta et al., 1987).

 Oogenesis-Flight Syndrome in Brown Planthoppers (Nilaparvata lugens):

Fig. 13 Two brown planthoppers (Nilaparvata lugens) on a stem. [Taken by Sylvia Villareal, 2008. https://www.flickr.com/photos/ricephotos/4270847124]

Fig. 14 Different morphologies of wing size for the brown planthopper (Nilaparvata lugens) [Adapted by Lin et al., 2015]

Migration and reproduction are 2 very energetically demanding events. For species that experience both, it is impossible to allocate enough resources to both events without any making any compensations. This results in a dilemma called the oogenesis-flight syndrome and has been observed in many species and animals such moths, crickets, aphids, birds, and others (Lin et al., 2016). To survive, species must find a way to work around this problem.

Researchers have discovered a special adaptation in brown planthopper species to adapt to the lack of total necessary resources. This rice-feeding pest uses gene expression to vary the wingspan in its larva based on the environmental conditions (Lin et al., 2016). In return, reproduction will be favored for planthoppers with short wings, or migration for long wings, which allows the species to allocate its resources meaningfully (Lin et al., 2016). This multigenerational phenomenon is called polyphenism (Lin et al., 2016).

In a population of planthoppers, assuming that the rice crops are healthy, planthoppers will mostly express short wings until the population size reaches its carrying capacity. This occurs because they do not need to migrate, and keeping short wings allows them to focus their resources on reproduction and grow the colony. Past the carrying capacity, the available resources will diminish, and as the colony is forced to migrate, larva will express long wings, and won’t have the same reproductive capabilities as their predecessors. Once they find a new home with an abundance of resources, short wings will be expressed in the new generation and the cycle repeats. Other factors can also force long-winged expression and migration in the species such as rotten rice, important temperature fluctuations and competition (Lin et al., 2016).

More specifically, this morphing phenomenon is controlled by the insulin pathway of the insect (Lin et al., 2016). An important gene involved is the FOXO gene, a forkhead gene in planthoppers that inhibits the insulin pathway and inhibits growth (Lin et al., 2016). Essentially, FOXO proteins are transcription factors which are necessary for gene expression and DNA replication. Other important proteins are PI3K, PDK1 and Akt which inhibit FOXO through the Akt/Pkb signaling pathway, thereby activating growth (Lin et al., 2016). In nature, these pathways are controlled by external environmental signals. Lin et al. (2016) simulated natural conditions and tested whether these genes influence wingspan growth or not. They used the pharmaceutical drug Perifosine which inhibits the Akt/Pkb pathway (Lin et al., 2016). Effectively, it was shown that inhibition of this pathway led to shorter wings and inhibition of FOXO led to longer wings in the brown planthoppers (Lin et al., 2016). In other words, these pathways control cell replication and growth of wing tissue, and that their response to the environment of brown planthopper dictates the expression of wingspan of next generation larva.

Fig. 15 Activation (left) and inhibition (right) of the Akt/Pkb pathway leading to inhibition or activation of FOXO pathway respectively. [Adapted by Lin et al., 2016]

Lastly, Lin et al. (2015) conducted another study showing that injuries inflicted on mother planthoppers would result in short wings of nymphs. Again, the FOXO insulin pathway is inhibited in this case to decrease the wingspan (Lin et al., 2015). Little is understood for why this mechanism occurs. It could be that shorter wings in nymph simply result from the healing pathways being activated. But it was also suggested that this occurrence could be a beneficial adaptation; injured wings is a sign of poorer health in the colony and favoring reproduction over migration in the next generations of planthoppers could be an applied method for attempting to save the colony (Lin et al., 2015).

Conclusion

Throughout this essay we have shown the complexity of migration and determine that a variety of external and internal factor affects animal migration. From hormonal changes affecting salmons, too transitioning between different ecosystem or even the adaptation of the eel’s body to the salinity of water the example is diverse. However, the conclusion stays the same, animal migration is partially governed by a variety of chemical phenomenon between the organisms and their respective environment, this chemical reaction can vary from chemotaxis, hormone regulation or even osmoregulation. Therefore, a deeper understanding of these chemical phenomenon’s gives us more insight on the driving factor behind animal migration. 

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