Potamopyrgus antipodarum

Deanna M. Soper, Ph.D.

Assistant Professor of Biology, University of Dallas, Irving, Texas

Fig. 1. Male Potamopyrgus antipodarum.

Fig. 1. Male Potamopyrgus antipodarum.

In the Northern Hemisphere, the month of January means colder temperatures and shorter days, while in the Southern Hemisphere, where the Taxon of the Month is native, it is summer. Potamopyrgus antipodarum is a small (2–5mm), freshwater snail species native to New Zealand and can be quite abundant in lakes and streams on both the North and South Islands of New Zealand. This species is being used across the world to answer a wide variety of different biological questions including: the evolution of sexual reproduction, evolutionary genetics, ecotoxicology, invasive biology, and reproductive behavioral evolution. Its current range includes not only New Zealand, but also invasive populations across Europe and North America. Potamopyrgus antipodarum, sometimes referred to as the New Zealand Mud Snail, was first described by John Edward Gray in 1843 and later characterized by Michael Winterbourn (1970, 1972). In 1974, Michael Winterbourn documented infection of the snails by several sterilizing trematode parasites (worms), but one genus, Microphallus, is particularly common in lake populations (Lively, 1987).  This sterilizing trematode first infects snail hosts, where the parasite develops into cercariae. Infected snails are then eaten by ducks where the parasite develops into the adult worm stage. The worms undergo sexual reproduction whereby eggs are produced and then released with the duck’s feces. This gives the snails an opportunity to eat the eggs and become infected with the parasite starting the life cycle over again.

Reading about this snail, the famed evolutionary biologist John Maynard Smith (1978) proposed that this species could serve as a model system to solve a long-standing riddle: the evolution of sex. Why sexual reproduction evolves and persists in populations has been a question since Charles Darwin’s time. In 1859, Darwin published the first edition of On the Origin of Species and in it expressed doubt that long-standing asexual lineages existed when he said that “Finally then, we may conclude that in many organic beings, a cross between two individuals is an obvious necessity for each birth; in many others it occurs perhaps only at long intervals; but in none, as I suspect, can self-fertilisation go on for perpetuity.” (Darwin, 1859, page 101). Sexual females are required to produce males, which means that they have a reduced growth rate compared to asexual females because males cannot produce offspring (see figure 1). This means that all else being equal, asexual females should take over sexual females in the same population quickly. And yet, sexuality is ubiquitous among all higher order plants and animals. 

Fig. 2. Sexual reproduction versus asexual reproduction. Color representative of genetic background.

Fig. 2. Sexual reproduction versus asexual reproduction. Color representative of genetic background.

This snail species provides an ideal opportunity to provide answers to the question of sex because many endemic populations contain ecologically non-distinct sexual and asexual lineages. Consequently, Curtis Lively (1987) launched P. antipodarum as system for use in the field of evolutionary biology when he sought to answer the question of why sexual reproduction evolves and is maintained in populations over time. In the early 1990’s it was discovered that some snails contain two copies of each chromosome (diploid) and are sexual – females produce on average 50% female, 50% male. While other snails contain three copies of each chromosome (triploid) and are asexual – females produce mostly all females (Wallace, 1992). Since then, snail populations containing up to six copies of each chromosome have been discovered (Neiman et al., 2011). 

Research on the relationship between the snail and the sterilizing trematode parasite has found a strong positive association between presence of parasites and presence of males, which is a measurement of the percent of snails in a population that are sexual (Lively, 1987; Jokela, 2009; King et al., 2011). This means that where there are parasites that coevolve with their hosts, there is sexual reproduction. Sexuality is favored in environments with coevolving parasites because sexual lineages generate genetic diversity in each generation, while asexual females produce offspring that are 100% related. The sexual portions of the population are a “moving target” and the asexual lineages are a “static target” resulting in parasites more easily evolving the ability to infect asexual lineages. Parasites keep the asexual populations “in check” allowing the sexuals to remain in the population. 

Fig. 3. Baby snail just born.

Fig. 3. Baby snail just born.

Although some biological and ecological characteristics of the snail have been documented, other aspects remain a mystery. For example, it is not known what determines that a snail embryo will develop into a male vs a female adult snail. The sexual life of this species is unique because unlike most snails that lay eggs, P. antipodarum female snails undergo “pregnancy” (internal gestation) and give live birth (see Fig. 3 of baby snail just born). Occasionally, baby snails can be born inside their gestational sac (see video below). Males can be identified by external genitalia that they use to fertilize sexual females (Fig. 1). A male can initiate mating by crawling on top of a female at which time the female can reject the male mating attempt by vigorously shaking her shell back and forth to knock the male off. Recent research has found that females can be choosey, but what females pay attention to during mating attempts and what causes females to prefer particular males also remain unanswered questions. This little snail has provided important insights to evolutionary biology, ecology, and reproductive biology, but still holds the answer to many questions that need to be explored.

Potamopyrgus antipodarum born in gestational sac.  Video Credit: Deanna Soper

Deanna Soper is an Assistant Professor of Biology at the University of Dallas where she uses P. antipodarum to understand how parasitic selective pressure and host/parasite coevolution influences the evolution of reproductive behaviors. Her lab website can be found here.

References

Darwin, C. R. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London: John Murray. (1st edition).

Jokela, J., M. F. Dybdahl and C. M. Lively. 2009. The Maintenance of Sex, Clonal Dynamics, and Host-Parasite Coevolution in a Mixed Population of Sexual and Asexual Snails. 174: S43–S53.

King, K. C., L. F. Delph, J. Jokela and C. M. Lively. 2011. Coevolutionary hotspots and coldspots for host sex and parasite local adaptation in a snail-trematode interaction. Oikos. 120: 1335–1340.

Lively, C. M. 1987. Evidence from a New Zealand snail for the maintenance of sex by parasitism. Nature. 328: 519–521.

Maynard Smith, J. 1978. The Evolution of Sex. Cambridge University Press. Cambridge.

Neiman, M., D. Paczesniak, D. M. Soper, A. T. Baldwin and G. Hehman. 2011. Wide Variation in Ploidy level and Genome Size in a New Zealand Freshwater Snail with Coexisting Sexual and Asexual Lineages. Evolution. 65: 3202–3216.

Wallace, C. 1992. Parthenogenesis, Sex and Chromosomes in Potamopyrgus. Journal of Molluscan Studies. 58: 93–107. 

Winterbourn, M. J. 1970.  Population Studies on the New Zealand Freshwater Gastropod, Potamopyrgus antipodarum (Gray).  Journal of Molluscan Studies39: 139–149.

Winterbourn, M. J. 1972. Morphological Variation of Potamopyrgus jenkinsi (Smith) from England and a comparison with the New Zealand species, Potamopyrgus antipodarum (Gray).  Proceedings of the Malacological Society London. 40: 133.

Winterbourn, M. J. 1974.  Larval Trematoda Parasitising the New Zealand Species of Potamopyrgus (Grstropodoa: Hydrobiidae). Mauri Ora. 2: 17–30.

Cannabis

Daniela Vergara

Postdoctoral Fellow, University of Colorado, Boulder, CO, U.S.A.

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We end the year with the plant genus Cannabis, belonging to the family Cannabaceae, which also includes hops (Humulus sp.) and Hackberries (Celtis). Cannabis is most famous today for its use as a recreational drug, aka marijuana, although the legalization of this plant as a drug has been quite controversial in the United States and across the world. Despite its notoriety, however, the origins, chemical properties, reproductive strategies and dispersal of Cannabis across the globe are quite fascinating and this plant genus has been impacting human culture for ages. Cannabis is one of the oldest domesticated plants and various ancient human cultures have used it for spiritual rituals, medicinal purposes, and fiber for rope or clothing that has been extracted from hemp plants (Li 1973, 1974; Russo, 2007, 2008). The genus most likely originated in Central, South or Eastern Asia but the exact origin of Cannabis is difficult to determine because of shifts in its distribution between glacial cycles (Clarke & Merlin 2013). Humans brought this species to Europe and later to Africa and the Americas where it was cultivated and domesticated into different varieties (Clarke & Merlin 2013). 

Carolus Linnaeus, the founder of the binomial species system, was the first person to classify the Cannabis genus in 1753, and only identified a single species, Cannabis sativa L. However, Jean Baptiste Lamarck (yes, the one who came up with a first theory of adaptation, now known and disregarded as “Lamarckian evolution”) described a second species, Cannabis indica, in 1785 (Watts, 2006). While the validity of the second species is debated, the groupings “sativa” and “indica” are still commonly used. Interestingly, Cannabis has an unusual amount of genetic diversity when compared to other plant groups (Sawler et al. 2015; Lynch et al. 2016; Vergara et al. 2016). Recent scientific research has found that there are genetic clusters, and thus it is possible that several other species will be described. However, these do not seem to reflect Lamarck’s classification of C. sativa and C. indica (Sawler et al. 2015; Lynch et al. 2016; Vergara et al. 2016). 

What molecular properties and processes make this plant so popular as a recreational drug? Cannabis produces cannabinoids, which interact with our own endocannabinoid system within the brain and nervous system (Gertsch 2008). The endocannabinoid system is involved in regulating multiple physiological processes, including sleep and hunger. One of the primary and most widely known cannabinoids produced by the Cannabis plant is Δ-9-tetrahydrocannabinolic acid (THCA), which is converted to the neutral form Δ-9-tetrahydrocannabinol (THC) once heated. This neutral form interacts with the endocannabinoid system producing a psychoactive effect (gets us “high”). THC also seems to have important medical uses potentially serving as treatment for Parkinson’s disease (Carrol et al. 2012), dementia (Walther et al. 2006), and autoimmune disorders (Lyman et al. 1989). The other well-known cannabinoid in Cannabis is cannabidiolic acid (CBDA), which produces cannabidiol (CBD) when heated. Data suggest CBD, which is not psychoactive, may mitigate some of the negative effects of THC (such as anxiety and paranoia) and has potential uses in treating cancer (Soliman et al. 2015) and epilepsy (Mechoulam et al. 2002; Devinsky et al. 2014). Besides THC and CBD, Cannabis produces around 74 different cannabinoids (ElSohly et al. 2005; Radwan et al. 2008; ), which are present at varying potencies and ratios across particular cultivars and may also have medical importance, including cannabigerol (CBG) Borelli et al., 2014), cannabichrome (CBC) (Izzo et al. 2012) and Δ-9-tetrahydocannabivarin (THCV) (McPartland et al. 2015).

Cannabis also has interesting reproductive strategies. It can be either dioecious, meaning that there are male and female plants, similar to what we see in humans and other animals (Soltis et al. 2005; Bell et al. 2015). However some Cannabis varieties are monoecious, and thus produce both males and female flowers in the same plant. To make this even more confusing, when environmentally stressed, some male plants can produce female flowers and some female plants can produce male flowers. Additionally, sex is determined by two chromosomes, X and Y (thus males are XY and females are XX), but the hermaphrodites have undifferentiated chromosomes (Hirata 1929; Yamado 1943; Sakomoto et al. 1998). Interestingly, males, females and hermaphrodites can cross with each other and produce fertile offspring.

About the Author

Dr. Daniela Vergara is post-doctoral researcher at the University of Colorado, Boulder, where she is working in Dr. Nolan Kane’s lab Cannabis Genomic Research Initiative. Specifically, Daniela has been exploring the cannabinoid genes in the genome and understanding the how these genes relate to the chemotypes. Daniela also founded and is the director of a non-profit organization The Agricultural Genomics Foundation that holds a 501(C)(3) status (AGF; AgriculturalGenomics.org) and aims in becoming a genomic repository (“library of genomes”) helping CGRI perform their research. AGF also educates the public about science, Cannabis, evolutionary biology, and genomics, through public talks.

References

Bell, C. D., D. E. Soltis & P. S. Soltis. 2010. The age and diversification of the angiosperms re-revisited. American Journal of Botany 97: 1296–1303.

Borrelli, F., E. Pagano, B. Romano, S. Panzera, F. Maiello, D. Coppola, L. De Petrocellis, L. Buono, P. Orlando & A. A. Izzo. 2014. Colon carcinogenesis is inhibited by the TRPM8 antagonist cannabigerol, a Cannabis-derived non-psychotropic cannabinoid. Carcinogenesis 35: bgu205.

Carroll, C. B., M‐L. Zeissler, C. O. Hanemann & J. P. Zajicek. 2012. Δ9‐tetrahydrocannabinol (Δ9‐THC) exerts a direct neuroprotective effect in a human cell culture model of Parkinson's disease. Neuropathology and Applied Neurobiology 38: 535–547.

Clarke, R. C. & M. D. Merlin. 2013. Cannabis: evolution and ethnobotany. University of California Press.

Devinsky, O., M. R. Cilio, H. Cross, J. Fernandez‐Ruiz, J. French, C. Hill, R. Katz, V. Di Marzo, D. Jutras‐Aswad, W. G. Notcutt & J. Martinez‐Orgado. 2014. Cannabidiol: pharmacology and potential therapeutic role in epilepsy and other neuropsychiatric disorders. Epilepsia 55: 791–802.

ElSohly, M.A. & D. Slade. 2005. Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life sciences 78: 539–548.

Gertsch, J., M. Leonti, S. Raduner, I. Racz, J.-Z. Chen, X.-Q. Xie, K.-H. Altmann, M. Karsak & A. Zimmer. 2008. Beta-caryophyllene is a dietary cannabinoid. Proceedings of the National Academy of Sciences 105: 9099–9104.

Hirata, K. 1929: Cytological basis of the sex determination in Cannabis sativa. Idengaku Zasshi. 4: 198–201.

Izzo, A. A., R. Capasso, G. Aviello, F. Borrelli, B. Romano, F. Piscitelli, L. Gallo, F. Capasso, P. Orlando & V. Di Marzo. 2012. Inhibitory effect of cannabichromene, a major non‐psychotropic cannabinoid extracted from Cannabis sativa, on inflammation‐induced hypermotility in mice. British journal of Pharmacology 166: 1444–1460.

Li, H. L. 1973. An archaeological and historical account of cannabis in China. Economic Botany 28: 437–448.

Li, H. L. 1974. Origin and use of Cannabis in Eastern Asia; Linguistic-cultural implications. Economic Botany 28: 293–301.

Lyman, W. D., J. R. Sonett, C. F. Brosnan, R. Elkin & M. B. Bornstein. 1989. Δ 9-tetrahydrocannabinol: a novel treatment for experimental autoimmune encephalomyelitis. Journal of neuroimmunology 23: 73–81.

Lynch, R. C., D. Vergara, S. Tittes, K. White, C. J. Schwartz, M. J. Gibbs, T. C. Ruthenburg, K. deCesare, D. P. Land & N. C. Kane. 2016. Genomic and Chemical Diversity in Cannabis. Critical Reviews in Plant Sciences 35: 349–363.

McPartland, J. M., M. Duncan, V. Di Marzo & R. G. Pertwee. 2015. Are cannabidiol and Δ9‐tetrahydrocannabivarin negative modulators of the endocannabinoid system? A systematic review. British journal of pharmacology 172: 737–753.

Mechoulam, R., L.A. Parker & R. Gallily. 2002. Cannabidiol: an overview of some pharmacological aspects. The Journal of Clinical Pharmacology 42: 11S-19S.

Radwan, M. M., S. A. Ross, D. Slade, S. A. Ahmed, F. Zulfiqar & M. A. ElSohly. 2008. Isolation and characterization of new Cannabis constituents from a high potency variety. Planta medica 74: 267–272.

Russo, E. B. 2007. History of Cannabis and its preparations in saga, science, and sobriquet. Chemistry & Biodiversity 4: 1614–1648.

Russo, E. B., H. E. Jiang, X. Li, A. Sutton, A. Carboni, F. Del Bianco, G. Mandolino, D. J. Potter, Y. X. Zhao, S. Bera & Y. B. Zhang. 2008. Phytochemical and genetic analyses of ancient cannabis from Central Asia. Journal of Experimental Botany 59: 4171–4182.

Sakamoto, K., Y. Akiyama, K. Fukui, H. Kamada & S. Satoh 1998. Characterization; Genome Sizes and Morphology of Sex Chromosomes in Hemp (Cannabis sativa L.). Cytologia 63: 459–464.

Sawler, J., J. M. Stout, K. M. Gardner, D. Hudson, J. Vidmar, L. Butler, J. E. Page & S. Myles. 2015. The Genetic Structure of Marijuana and Hemp. PloS One 10: e0133292.

Solinas, M., V. Cinquina & D. Parolaro. 2015. Cannabidiol and Cancer—An Overview of the Preclinical Data. In Molecular Considerations and Evolving Surgical Management Issues in the Treatment of Patients with a Brain Tumor. InTech.

Soltis, D. E., P. S. Soltis, P. K. Endress & M. W. Chase. 2005. Phylogeny and evolution of angiosperms. Sinauer Associates Incorporated.

Walther, S., R. Mahlberg, U. Eichmann & D. Kunz. 2006. Delta-9-tetrahydrocannabinol for nighttime agitation in severe dementia. Psychopharmacology 185: 524–528.

Watts, G. 2006. Science commentary: Cannabis confusions. BMJ: British Medical Journal 332: 175.

Vergara, D., H. Baker, K. Clancy, K. G. Keepers, J. P. Mendieta, C. S. Pauli, S. B. Tittes, K. H. White & N. C. Kane. 2016. Genetic and Genomic Tools for Cannabis sativa. Critical Reviews in Plant Sciences 35: 364–377.

Yamada, I. 1943. The sex chromosome of Cannabis sativa L. Seiken Ziho2: 64–68.

Myxozoa

Jonathan Foox

Postdoctoral Associate, Institute for Computational Biomedicine, Weill Cornell Medicine, New York, New York

Taxonofthemonth_myxozoan_diversity.png

This month's featured taxon is Myxozoa: a bizarre, poorly understood group of microscopic, obligate parasites. Members of this taxon are typically found parasitizing teleost fish and annelid worms, though they have been observed in a wide spectrum of hosts including amphibians, birds, bryozoans, cephalopods, reptiles, shrews, and waterfowl. These parasites are globally distributed in marine and freshwater aquatic environments (though some are exclusively terrestrial), and have been found in nearly all tissue and organ types. Myxozoa is an extremely diverse group not only in distribution but in species richness, comprising over 2,200 described species distributed among over 60 genera (Lom and Dyková, 2006) – which likely represents a small fraction of the total diversity, with some estimates of 16,000 species in the Neotropics alone (Naldonia et al., 2011).

Although most myxozoan infections are innocuous, some species are well known pathogens that cause fatal diseases that can have significant economic impact, particularly on fish farms (Kent et al., 2001). One especially nasty example is Tetracapsuloides bryosalmonae, the causative agent of Proliferative Kidney Disease, which can wipe out 90% of infected salmonid populations, and even caused authorities to shut down a 183-mile stretch of Yellowstone River last summer (Young, 2016).

Each individual myxozoan has a fantastically complex life cycle that involves radical physiological transformations. Upon penetration of a host, an individual amoeboid-like reproductive body will undergo complex rounds of cellular fusion and division, before ultimately producing a reproductive spore that will eventually emerge from its host into the water column in search of its next host. These spores exhibit a stunningly diverse array of morphologies, including spherical, fusiform, pyriform, floral, round, ovoid, flattened, elongated, with or without caudal appendages, and all variations exhibit a wide variety of variation in orientation and number of constituent parts. The image gives just a taste of the incredibly morphological diversity of this taxon. In rather dramatic fashion, these spores harbor a complex organelle known as a polar capsule, which contains a coiled up filament that, upon stimulation, will rapidly evert from the capsule like the finger of a glove. The sticky filament flies through the water and latches onto the integument of the target animal like a grappling hook, allowing the spore to wriggle its way into its next host and beginning the parasitic cycle anew.

But perhaps the most impressive thing about Myxozoa is its position within the tree of life. These microscopic, morphologically simplistic parasites are members of the phylum Cnidaria, the lineage containing animals such as jellyfish, sea anemones, and corals. Indeed, myxozoans are extremely divergent, incredibly reduced, highly derived evolutionary cousins of these commonly known creatures. And this relationship of myxozoans to its cnidarian allies renders the group one of the most dramatically degenerate parasitic radiations known to biology. Myxozoans have neither tentacles, nor gastrovascular cavities, nor even tissue layers – and yet, they are cnidarians, by virtue of their polar capsules, which are homologous to cnidocytes (the stinging organelles only found within Cnidaria).

To put it into perspective: the size difference between an individual myxozoan spore and the common moon jelly is equivalent to the size difference between a human and Mt. Everest. Quite the difference.

And yet, this evolutionary relationship was not understood for nearly two hundred years. After first discovery in the early 19th century, myxozoans were categorized as various protistan lineages. Upon their confirmation as cnidarians not much more than 20 years ago (Siddall et al., 1995), biologists realized that myxozoans are not only incredibly derived cnidarians, but that they are the smallest and perhaps simplest animals in existence. Having lost nearly all diagnostic features known to animals (cellular structures such as centrioles and cilia), myxozoans stretch the very limit of what we understand to be "animals". It is only fitting that we save for the end of the year a taxon that stretches the limits of our biological imagination.

References

Kent, M.L., K.B. Andree, J.L. Bartholomew, M. El-Matbouli, S.S. Desser, R.H. Devlin, S.W. Feist, P.P. Hedrick, R.W. Hoffmann, J. Khattra, S.L. Hallett, R.J.G. Lester, M. Longshaw, O. Palenzeula, M.E. Siddall ME & C.X. Xiao. 2001. Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol  48: 395–413.

Lom, J., & I. Dykova. 2006. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitology 53: 1-36. London, pp. 115–154.

Naldonia, J., S. Aranab, A.A.M. Maiac, M.R.M. Silvac, M.M. Carrieroc, P.S. Ceccarellid, L.E.R. Tavarese & E.A. Adrianof. 2011. Host–parasite–environment relationship, morphology and molecular analyses of Henneguya eirasi n. sp. parasite of two wild Pseudoplatystoma spp. in Pantanal Wetland, Brazil. Veterinary Parasitology 177: 247–255.

Siddall, M.E., D.S. Martin, D. Bridge, S.S. Desser & D.K. Cone. 1995. The demise of a phylum of protists: phylogeny of Myxozoa and other parasitic Cnidaria. Journal of Parasitology 81: 961–967.

Young, Ed.  2016.  A Tiny Jellyfish Relative Just Shut Down Yellowstone River.  The Atlantic: https://www.theatlantic.com/science/archive/2016/08/the-parasite-that-just-shut-down-a-montana-river-has-an-unbelievable-origin/496817/ .

Philcoxia

Ricardo Bressan Pacifico

Ph.D. Student, Plant systematics and biogeography lab - Maringá State University, Maringá, Brazil

Photo credit. A. V. Scatinga.

Photo credit. A. V. Scatinga.

With Halloween just around the corner, our taxon of the month is a recently described and unique genus of plants with unusual feeding habits, Philcoxia. This genus was first described 17 years ago, known only from three species (Taylor & Souza, 2000), although since then several additional species were recently discovered bringing the number of species in the genus to seven (Scatigna et al., 2015; 2017). All Philcoxia species are rare and are endemic to central Brazilian mountaintop grasslands, usually known as campo rupestre (Taylor & Souza, 2000). They are annual herbs, usually less than 30 cm tall, with delicate roots and stems, and small white to purple flowers measuring less than 1 cm in length. However, the most striking features of Philcoxia took more than a decade to be discovered. All species have underground leaves to which many nematodes attach and these leaves look somewhat similar to those found in carnivorous plants, a feature which caught the attention of researchers from California and Brazil, who decided to perform carnivory tests (Fritsch et al., 2007). The initial carnivory test results were negative (Fritsch et al., 2007), however, a few years later, a new and creative experiment shed light on this matter. In this experiment, radioactive nitrogen (15N) was used to feed bacteria (Escherichia coli) that were fed to to a population of nematodes (Caenorhabdtis elegans), which, in turn, were placed over the underground leaves of Philcoxia minensis for two days. The idea was to track the nutrient acquisition of Philcoxia, i. e., to see if the radioative nitrogen from nematodes would somehow be absorbed by this plant. The fast absorption of the 15N revealed by the elevated concentration of it in Philcoxia leaves strongly suggested that the nematodes were digested (instead of naturally decomposed) and absorbed by Philcoxia leaves (Pereira et al. 2012)⁠ suggesting that this genus of plants is carnivorous and feeds on nematodes. Carnivory evolved at least six times within angiosperms (flowering plants) and about 20 carnivorous genera distributed in 10 distinct families have been identified. A general cost–benefit model predicts that carnivory will be restricted to well lit, low-nutrient areas, where the major source of important nutrients such as nitrogen and phosphorus will be obtained from captured and digested invertebrates (Pereira et al. 2012).⁠ Philcoxia, like other carnivorous plants, live in nutrient-poor soils and are the only known carnivorous plants in the Plantaginaceae family (Pereira et al. 2012). The unusual new mechanism of carnivory discovered in Philcoxia caught public attention in high impact scientific journals such as Nature (Rowland, 2012).

References

Fritsch, P. W., F. Almeda, A. B. Martins, B. C. Cruz and D. Estes. 2007. Rediscovery and phylogenetic placement of Philcoxia minensis (Plantaginaceae), with a test of carnivory. Proceedings of the California Academy of Sciences 58: 447–467

Pereira, C. G., D. P. Almenara, C. E. Winter, P. W. Fritsch, H. Lambers and R. S. Oliveira. 2012. Underground leaves of Philcoxia trap and digest nematodes. Proc. Natl. Acad. Sci. U. S. A. 109: 1–5. doi:10.1073/pnas.1114199109.

Rowland, K. 2012. Hungry plant traps worms underground. Nature (news). doi:10.1038/nature.2012.9757

Scatigna, A. V., V. C. Souza, C. G. Pereira, M. A. Sartori, and A. O. Simoes. 2015. Philcoxia rhizomatosa (Gratioleae, Plantaginaceae): A new carnivorous species from Minas Gerais, Brazil. Phytotaxa 226: 275–280

Scatigna, A. V., Silva, N. G., Alves, R. J. V., Souza, V. C. and O. Simões. 2017. Two New Species of the Carnivorous Genus Philcoxia (Plantaginaceae) from the Brazilian Cerrado. Systematic Botany 42:351-357. doi: 10.1600/036364417X695574

Taylor, P., Souza, V. C., Giulietti, A. M. and R. M. Harley. 2000. Philcoxia: A new genus of Scrophulariaceae with three new species from eastern Brazil. Kew Bulletin 55: 155–163. 

Enterobacteriaceae

Stephanie F. Loria

We have been pretty biased towards multicellular organisms in the Taxon of the Month posts. But this month, we are doing justice to our single-celled organism friends giving them the recognition they deserve as they are so crucial to the health of all multicellular life. For September, we focus our attention on the bacteria family, Enterobacteriaceae. Enterobacteriaceae are quite diverse and include more than 200 species in 51 genera (Octavia & Lan 2014; Janda & Abbott 2015). All Enterobacteriaceae are gram-negative, meaning that they possess a thin peptidoglycan layer in their cell walls causing them to appear pink after Gram staining (Beveridge 2001). Some well-known Enterobacteriaceae members include the medically important Escherichia coli, Salmonella and Klebsiella (Janda & Abbott 2015). E. coli is an essential human gut bacterium that can also act as a pathogen under certain conditions (Janda & Abbott 2015). Salmonella is notorious for causing illness of the human digestive system, which is sometimes fatal, and is transmitted through food and water contaminated with feces (Janda & Abbott 2015). Klebsiella species are found free-living in soil or water or in vertebrate digestive systems but are also responsible for a number of human illnesses including urinary tract infections and pneumonia.

Bacteria from the gastrointestinal tract of Narceus americana. Photo credit to C. Wright.

Bacteria from the gastrointestinal tract of Narceus americana. Photo credit to C. Wright.

Many organisms rely on gut-inhabiting bacteria to assist with the digestion of various foods. For example, detritivores, organisms that eat decaying organic matter in the soil, rely on bacteria for assistance in breaking down hard-to-digest plant material, such as cellulose (Taylor 1982). Many Enterobacteriaceae inhabit animal digestive systems and are known to assist with digestion (Lauzon et al. 2003). For a class project as an undergraduate, a fellow student (C. Wright) and I agar plated the gut contents of a common detritivore, the large North American millipede, Narceus americanus. After sequencing the 16S rRNA gene of the plated bacterial colonies, we discovered several members of Enterobacteriaceae inhabiting this millipede's gut including Bacillus mycoides, Serratia sp. and Enterobacter cloacae. All three of these bacteria were previously known to inhabit animal digestive tracts. B. mycoides was previously found in both the soil (Lewis 1932) and in earthworm guts (Jensen et al. 2003). Enterobacter cloacae is known from plants and insect digestive systems (Watanabe & Sato, 1998). Serratia has been recorded in the digestive tract of flies in the genus Dacus (Lloyd et al., 1986). It is possible that these bacteria are assisting this millipede species digest its food.

Several studies have examined the diversification of Enterobacteriaceae. Research indicates that the evolution of endosymbiotic forms occurred multiple times in this family (Husník et al. 2011). Additionally, many endosymbiotic Enterobacteriaceae coevolved with their hosts (Duchaud et al. 2003; Moran et al. 2005). Given their species diversity and the wide range of hosts they inhabit, Enterobacteriaceae are great organisms to study for understanding selective pressures on symbiotic relationships.

References

Beveridge, T.J. 2001. Use of the gram stain in microbiology. Biotechnic & Histochemistry 76: 111–118.

Duchaud, E., C. Rusniok, L. Frangeul, C. Buchrieser, A. Givaudan, S. Taourit, S. Bocs, C. Boursaux-Eude, M. Chandler, C. Jean-Francois and E. Dassa. 2003. The genome sequence of the entomopathogenic bacterium Photorhabdus luminescensNature biotechnology 21: 1307–1313.

Husník, F., T. Chrudimský & Václav Hypša. 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC biology 9: 87.

Janda, J.M. & S.L. Abbott. 2015. The family Enterobacteriaceae. Practical handbook of microbiology (Goldman, Emanuel and L. H. Greens, eds) 307–319.

Jensen, G.B., B.M. Hansen, J. Eilenberg & J. Mahillon. 2003. The hidden lifestyles of Bacillus cereus and relatives. Environmental microbiology 5: 631–640.

Lauzon, C. R., T. G. Bussert, R. E. Sjogren & R. J. Prokopy. 2003. Serratia marcescens as a bacterial pathogen of Rhagoletis pomonella fies (Diptera: Tephritidae). European Journal of Entomology 100: 87–92.

Lundgren, J. G., R. Michael Lehman & J. Chee-Sanford. 2007. Bacterial communities within digestive tracts of ground beetles (Coleoptera: Carabidae). Annals of the Entomological Society of America 100: 275–282.

Lewis, I.M. 1932. Dissociation and life cycle of Bacillus mycoides. Journal of bacteriology 24: 381–421.

Llyod, A.C., R.A.I. Drew, D.S. Teakle & A.C. Hayward. 1986. Bacteria associated with some Dacus species (Diptera: Tephritidae) and their host fruit in Queensland. Australian Journal of Biological Scienes 39: 361–368.

Moran, N.A., J.A. Russell, R. Koga and T. Fukatsu. 2005. Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Applied and Environmental Microbiology 6: 3302–3310. 

Octavia, S. & R. Lan. 2014. The family enterobacteriaceae. The Prokaryotes: Gammaproteobacteria 225–286.

Taylor, E.C. 1982. Role of aerobic microbial populations in cellulose digestion by desert millipedes. Applied and environmental microbiology 44: 281–291.

Watanabe, K. & M. Sato. 1998. Plasmid-mediated gene transfer between insect-resident bacteria, Enterobacter cloacae, and plant-epiphytic bacteria, Erwinia herbicola, in guts of silkworm larvae. Current Microbiology 37: 352–355.

Squirrels (Sciuridae)

Maurice Chen

Sciurus carolinensis. Photo credit to Maurice Chen.

Sciurus carolinensis. Photo credit to Maurice Chen.

I was walking through Madison Square Park earlier this week when I was stopped in my path by a rather outgoing bushy-tailed rodent. We stared at each other for several seconds, neither one of us willing to turn back down the road we traveled. After a short time time, I decided to circle around and continue along my path, the whole time being barraged with disgruntled chittering noises as I didn't pay the proper toll in nuts or whatever food I had on me. Because of my encounter, I decided that this month we honor the squirrelly members of the Sciuridae famly.

There are 286 known species within the Sciuridae family (Waldheim 1817) which can be further categorized into three groups. They are tree squirrels, ground squirrels, and flying squirrels.(Bradford 2014) The squirrels that we most commonly see in New York City are the tree squirrels, Sciurus carolinensis, or Eastern Gray Squirrels. Squirrels can be found throughout the world except in Australia. Squirrels primarily eat non-cellulose plant matter, such as seeds, fruits, and conifer cones, however they are also known to eat fungi and occasionally insects (Thorington & Ferrel 2006).

If you decide to enjoy your lunch in Madison Square Park, don’t be surprised if a squirrel casually walks up to you and patiently waits for a portion of your meal. It’s not uncommon to see squirrels in Madison Square Park perched on benches sharing french fries with a recent Shake Shack customer. However, you might notice that there is a particularly high population of squirrels running around compared to most years. This is the result of the 2016 mast year. A mast year is a period where oaks produce a much higher volume of acorns. Oaks can yield up to 10 times the amount they produce in an average year. Scientists hypothesize that masting developed as a way to guarantee propagation in the presence of high predation (Savage 2016). If acorns are produced in high quantities during certain years, some of the acorns will survive unscathed since the level of predators cannot consume the excess amount. This concept is called predator satiation. Mast years seem to occur irregularly and predicting when they might occur have eluded the best scientists. What makes squirrels special is that they can somehow predict when a mast year is about to occur and will also change their mating behaviors accordingly (Boutin et al. 2006). Before a mast year, female squirrels will produce a second litter of offspring since food sources will be plentiful in the upcoming mast. This allows squirrel to have an advantage over many of the other organisms that forage acorns.

Squirrels play an important role in genetic composition of oak forests due to their foraging behaviors. Squirrels are more likely to bury, or “cache” acorns from red oaks while immediately eating acorns from white oaks. Red oak acorns tend to have a higher fat content and will last the winter before germinating in the spring. White oak acorns tend to germinate soon after falling from their parent tree and are sweeter, thus making them more ideal for immediate consumption. Squirrels will therefore cache red oak acorns up to 150 feet away from its parent tree resulting in expansive red oak forests with tight clusters of white oaks (Line 1999).

While acorns are the preferred food source for storing for the winter, squirrels will resort to other sources when acorn yields are low. Interestingly, squirrels will actually harvest fungi and dry them out into a jerky (Bittel 2014). Squirrels will also tap maple trees for their sap, eating the sugary syrup once the water content has evaporated (Roach 2005).

References

Bittel, J. 2014. 5 surprising facts about squirrels (hint: they make jerky). National Geographic

Boutin, S., L.A. Waters, A.G. McAdam, M. M. Humphries, G. Tosi & A. A. Dhondt. 2006. Anticipatory reproduction and population growth in seed predators. Science 314: 1928-1930

Bradford, A. 2014. Squirrels: diet, habits & other facts. Live Science

Line, L. 1999. When nature goes nuts: an astonishing array of animals is linked in some surprising ways to the mighty oak and its bounty. National Wildlife Federation

Roach, J. 2005. No nuts, no problem: squirrels harvest maple syrup. National Geographic

Savage, J. 2016. When is a tree smarter than a squirrel? Society for the Protection of New Hampshire Forests

Thorington, R. W. & K. Ferrell. 2006. Squirrels: the animal answer guide. John Hopkins University Press 75

Waldheim, F. 1817. Scuridae. Integrated Taxonomic Information System

Mountain Gorilla (Gorilla beringei beringei)

Harald Parzer

Dominant Silverback with wound due to a fight with a lone male. Photo credit to Harald Parzer.

Dominant Silverback with wound due to a fight with a lone male. Photo credit to Harald Parzer.

Mountain gorillas (Gorilla beringei beringei) are a subspecies of the Eastern Lowland Gorilla (Gorilla beringei) and are endemic to (or only found in) the mountainous region of the Albertine Rift in East Africa at an altitude from around 2200m to 4000m. They are found in two disjunct areas: the Virunga mountains, Rwanda and in Bwindi Impenetrable Forest, Uganda. Interestingly, these two populations behave quite differently. Bwindi Mountain Gorillas tend to climb much more and eat plenty of fruits, while the Virunga gorillas mostly stay on the ground and replace fruits with herbaceous stems. In fact, because of this, and morphological and genetic differences, some scientists argue that these populations represent two species, or at least two subspecies. Unfortunately, due to poaching and habitat destruction, only 880 individuals of this critically endangered species are left on this planet.

Mountain gorillas are incredibly powerful specimens to behold. They can grow to be as tall as an average man, with the same muscle and fat distribution, and weigh up to 430 lbs. Bodybuilders could only dream of such numbers. And yet, the mountain gorilla diet consist solely of plant matter! To maintain such weight, male mountain gorillas eat up to 34 kg of plants. Although they do not consume animal protein, about 18% of their overall food intake is protein from plant matter they select. Thus, an adult mountain gorilla can eat of up to 612 grams of protein every day far surpassing that of a bodybuilder's diet. Higher ranking females tend to have a higher caloric intake, not because they get nutrient richer plants, but because they tend to eat faster and are less active than their male counterparts.

Female mountain gorilla with her offspring. Photo credit to Harald Parzer.

Female mountain gorilla with her offspring. Photo credit to Harald Parzer.

Research shows that the home range of mountain gorillas changes with the seasons. In the dry season, mountain gorillas may increase their home ranges to 18 square miles in order to find their favorite plants (in Bwindi they have been observed to eat 107 species of plants). During the rainy season, the home ranges of mountain gorillas shrink dramatically as plants are more abundant and foraging doesn't require them to travel as far.

Mountain gorillas, which are either left or right handed in about the same proportions, live in small groups of around 10 individuals. The groups are composed of one to a few adult males, as well as females and juveniles of either sex. The dominant male, or silverback (named after his grey short hair on his back, which develops as a teenager), is almost twice as heavy as an adult female, and sires about 85% of the offspring if a second ranking silverback is in the group (who sires the remaining 15%). Thus, a silverback benefits from a large harem, as this means a lot of offspring. At times, like the group visited by the author in Bwindi Impenetrable Forest, older silverbacks are still hanging onto their group (and regularly get lost due to their slower pace...) and can be observed at the edge of it, old men observing the youth.

Infant mountain gorilla (about half a year old). Photo credit to Harald Parzer.

Infant mountain gorilla (about half a year old). Photo credit to Harald Parzer.

On average, a female produces 2.1–3.6 surviving offspring in her lifetime. Dominant females, which have higher lifespans, are producing more than lower ranking females. Infant mortality is high (21% of all infants won't make it to adulthood), mostly because of infanticide - yes, the ugly side of the mountain gorilla. When a new male takes over the group, after a vicious fights (see picture above) or natural death of the dominant silverback, the newcomer tends to kill all offspring to make sure that his harem is receptive for his own offspring. Thus, females prefer strong dominant males, which can protect their group as long as possible. Young males leave their groups when they are about 11 years old, and wander through the forest, mostly as lone males, to fight for a new group for themselves and that can take time.

Mountain gorillas, like all other gorillas, have not been observed to use tools in the wild, and have so far not been kept in zoos. Thus, if you want to meet this gentle giants, you will have to travel to Uganda or Rwanda, and join a gorilla trekking tour. The prices for such tours are steep ($600 for Bwindi National Park and $1500 for the Virunga Mountains), but they allow you to stay very close to one of the habituated groups for one hour. And you may even be hugged by a juvenile, as it happened to the trekking group of the author! These tours are well worth it and at least some of the money goes into protecting the habitat of the gorillas and to protecting other national parks, which are less frequently visited. So start saving money (cancel your TV subscription and write an essay for our upcoming competition to gain a few extra bucks), and get ready for a fantastic adventure! 

References

Bradley, B. J., M. M. Robbins, E. A. Williamson, H. D. Steklis, N. G. Steklis, N. Eckhardt, C. Boesch & L. Vigilant. 2005. Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proceedings of the National Academy of Sciences of the United States of America 102: 9418–9423.

Robbins, M. M., A. M. Robbins, N. Gerald-Steklis & H. D. Steklis. 2007. Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei). Behavioral Ecology and Sociobiology 61: 919–931.

Rothman, J. M., A. J. Plumptre, E. S. Dierenfeld, & A. N. Pell. 2007. Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. Journal of Tropical Ecology 23: 673–682.

Zihlman, A. L., & R. K. McFarland. 2000. Body mass in lowland gorillas: a quantitative analysis. American Journal of Physical Anthropology 113: 61–78.