Themes of Parasitology

Immigrants from Afar: Clonorchis sinensis

2012-02-27T10:38:00.000-05:00

Introduction:

Which trematode may cause serious disease, with loads ofover 25,000 parasites per patient? If you answered the Clonorchis sinensis, you are correct! Clonorchis sinensis, also known as the Chinese liver fluke, livesin the liver of humans and is commonly found in the bile ducts and gall bladder [1].The geographic distribution of this parasite is in endemic areas in Asiaincluding China, Japan, Korea, Taiwan, and Vietnam [1]. It is found mainly inAsian immigrants, or following ingestion of imported, undercooked, or pickledfreshwater fish. C.sinensis has also been reported in non-endemic areas including the UnitedStates.

Figure 1. Clonorchis sinensis: Chinese liver fluke

http://www.suite101.com/view_image.cfm/2299692

Do Hyun Park, M. D., Ph. D. and Hyun-Young Son, M. D. from theNew England Journal of Medicine presented a clinical case dealing with the diseaseassociated with C. sinensis. Briefly,an elderly man reported fatigue, fever, and abdominal pain for a week alongwith the consumption of raw pond smelt [2]. A duodenoscopy was performed andafter the cannulation of the common bile duct, numerous leaf-shaped worms poppedout (see video below)—subsequently identified as C. sinensis [2]. The wormburden and the duration of infection tend to reflect the clinical manifestationsof the disease clonorchiasis [2].

Video 1. Cannulation of the common bile duct displaying numerous trematode parasite C. sinensis being popped out of a patient with the disease clonorchiasis.

http://www.nejm.org/doi/full/10.1056/NEJMicm054461#t=article

Symbiont Description:

Clonorchis sinensisis a trematode in the phylum Platyhelminthes [3]. Because this parasite exhibitsa three-host sequence, part of its life cycle takes place in aquatic habitatswhile the other part takes place in terrestrial habitats. The physicalappearance of C. sinensis includesmany forms: egg, miracidium, sporocyst, redia, cercaria, metacercaria, andadult [3]. C. sinensis is classifiedas hermaphroditic; as a result, every single sexually mature form will produceeggs [3]. Interestingly, each adult yields a daily production of 4000 eggs forat least six months [3]! C. sinensis iscurrently infecting an estimated 30,000,000 humans and is believed to be thethird most prevalent trematode parasite in the world [3].

Host Description:

C. sinensisincludes three species of hosts: the mollusk, the fish, and the mammal. Eggsare evacuated with feces and ingested by a freshwater gastropod mollusk. A dozenspecies have been reported as vectors, but the most frequent one is Parafossarulus manchouricus [4].Numerous swimming larvae, also known as cercariae, are produced by asexualmultiplication and then leave the mollusk [4]. The cercariae penetrate avariety of fish species—almost a hundred—where they then encyst in the muscleas metacercariae [4]. Once the metacercariae are eaten by the fish, they excystin the mammal’s stomach and mature in the bile ducts of the liver [4].

Life Cycle:

DPDx—a websitedeveloped and maintained by CDC’s Division of Parasitic Disease and Malaria—providedan outstanding photo depicting the life cycle of C. sinensis. First, embryonated eggs are discharged in the biliary ductsof humans [1]. Second, eggs are ingested by a suitable snail intermediate host[1]. Each egg releases a miracidia, which go through four developmental stages:miracidia, sporocysts, rediae, cercariae [1]. The cercariae are then releasedfrom the snail and after a short period of free-swimming time in water, theycome in contact and penetrate the flesh of freshwater fish, where they encystas metaceriae [1]. After ingestion, the metacercariae excyst in the duodenumand ascend the biliary tract via the ampulla of Vater [1]. The cycle repeatsover and over again from this point on.

Figure 2. The three-host sequence life cycle of C. sinensis.

http://dpd.cdc.gov/dpdx/html/Clonorchiasis.htm

Ecology:

C. sinensis hashad large detrimental effects on humans, specifically those in areas such asAsia, where eating raw or undercooked fish is a part of their cultural upbringing.A human host with an average of infection will have or three dozen worms, andheavily infected individuals have been found with as many as 20,000 worms [3]. Theseparasites reside in the biliary system of the liver and occasionally in thepancreas. Although the liver or pancreas is not attacked, they are greatlydamaged due to the parasites’ migration through the biliary system [3]. Damagesinclude erosion of the epithelial lining of bile ducts, which leads to the developmentof blockage in the ducts due to the thickening of scar tissue [3]. This erosion,along with the effects of C. sinensis’perforation into the parenchyma of the liver leads to possible disturbance ofnormal hepatic functions [3].

An Example of the Three-Host Sequence:

Several unrelated species of hosts may be successivelyexploited as the parasite develops over its life cycle. The sequence of hostsconsists of the series of hosts utilized during the life cycle and is oftenreferred to as the longitudinal component of the cycle [4]. This sequence involvestwo dimensions: ecological (the succession of environments) and ontogenetic(the various developmental states of the parasites) [4]. The parasite undergoes ametamorphosis at each change of host because each time that the parasitechanges host, some genes are turned off while others are activated, resultingin a morphologically, anatomically, physiologically, and ethologically distinctorganism [4]. Adults of C. sinensisdemonstrate an example of the three-host sequence: the mollusk, the fish, andthe mammal.

References:

[1] Laboratory Identification of Parasites of Public Health Concern. “Clonorchiasis.”Centers for Disease Control and Prevention. Online. Accessed 24 Feb. 2012. <http://dpd.cdc.gov/dpdx/html/Clonorchiasis.htm>.

[2] Park, D. H. andH. Y. Son. “Images in Clinical Medicine: Clonorchis sinensis.” The New England Journal of Medicine. (2008);358: e18.

[3] Eckroad, E. and H. Lee. 2001. "Clonorchis sinensis."Animal Diversity Web. Online. Accessed 24 Feb. 2012. <http://animaldiversity.ummz.umich.edu/site/accounts/information/Clonorchis_sinensis.html>.

[4] Combes C. 2001. Parasitism: The Ecology and Evolution of IntimateInteractions. Chicago: University of Chicago Press. 36-38 p.

Fasciolopsis Buski- the giant fluke

2012-02-24T10:22:00.001-05:00

Introduction: Fasciolopsis Buski is commonly known as the giant fluke. It causes the disease fasciolpsiasis, which humans contract by consuming contaminated water plants. This disease can be asymptomatic if the parasite load is light. However, if the parasite load is heavy, then symptoms including abdominal pain, diarrhea, fever, swelling, and toxemia (toxins in the blood stream).¹

Symbiont Description: The genus name of this parasite is Fasciolopsis and it is a member of the trematode class. There are two members of the Fasciolopsis genus, but only one is pathogenic.

http://parasitology.webnode.com/medical/trematodes/fasciolopsis-buski/

Host Description:In the first stage of life, snails serve as hosts to the parasite. In the second stage, humans or pigs serve as the host when they consume water plants on which the metacercariae are encysted.

Life Cycle: Unembryonated eggs are laid in the intestine ofhumans or pigs. Eggs are passed in stool and are embryonated in water. Eggs hatch into miracidiae. The miracidae infect snails, where they develop into cercariae. Cercariae exit the snail and become free swimming, when they infectencyst as metacercariae on aquatic plants. Mammalian hosts become infected when the ingest the affected aquaticplants. ^1,2

http://www.dpd.cdc.gov/dpdx/html/fasciolopsiasis.htm

Ecology: F. buski is endemic to South Eastern Asia, where it is estimated to affect over 10 million people. Fasciolopsiasis can be diagnosed by identifying eggs in stool under a microscope. This disease is easily cured by praziquantel. The most effective way to prevent fasciolopsiasis infections is to boil water plants before consuming them. Drinking water should also be boiled or filtered in areas where sanitation is poor. Human and/or pig feces should not be used as fertilizer.²

^{An Example of Social Status:}

^{Individuals who are affected by fasciolopsiasis are generally in impoverished areas of the world, where water sanitation is not at its best. Thus, the encounter filter is more open for these individuals than someone who lives in average America. People have fewer resources at lower quality, which increases their risk of infection. Education about sanitation could potentially lead to lower prevalence.}³

Resources
1.) http://www.parasitesinhumans.org/fasciolopsis-buski-intestinal-fluke.html
2.) http://www.dpd.cdc.gov/dpdx/html/fasciolopsiasis.htm
3.) Combes, Claude. Parasitology: The Ecology and Evolution of Intimate Interactions.

Trichomonas vaginalis

2012-02-22T10:18:00.003-05:00

Trichomonas vaginalis is a parasitic protozoan, and causes the sexually-transmitted disease known as trichomoniasis. T. vaginalis is also one of the leading causes of vaginitis. Trichomoniasis is thought, by the World Health Organization, to be the most prevalent protozoan infection in the world, with over 180 million cases annually, and over 5 million in North America. Though, according to the Department of Natural Resources, trichomoniasis is incredibly prevalent in birds, this blog will focus on the human aspect.

The following link willl take you to the State of Michigan DNR, which has conducted many studies on the effects of Trichomoniasis in birds.
[http://www.michigan.gov/dnr/0,4570,7-153-10370_12150_12220-27288--,00.html]

Please allow a brief disclaimer. I understand that this blog is not meant for those with weak stomachs, but the pictures associated with this STD are just generally unpleasant...trust me. I will post a couple of links in case you are interested.

This flagellated protozoan does not have a very complicated lifestyle. As a sexually-transmitted parasite, T. vaginalis lives within the urethra of an infected male, or within the lower genital tract of and infected woman. Because T. vaginalis has no cyst form, it cannot exist effectively outside of the host. It can live for only a day or so if submerged in water, semen, or urine. However, it indeed overcomes this fragile lifestyle by persisting via sexual transmission.

Two cultured examples of T. vaginalis. These protozoa use their multiple flagella for movement.
http://www.cdc.gov/std/trichomonas/STDFact-Trichomoniasis.htm

Contrasting the typical pattern of other parasites, men are LESS likely to develop trichomoniasis than women. Though testosterone typically serves as an immunosuppressant, women infected with T. vaginalis are more likely to develop trichomoniasis. Though, according to the CDC, about 3.7 million people are infected, only 30% or so actually show symptoms. It is not clear why a minority of those infected show symptoms, but perhaps that can be attributed to other characteristics discussed in class, such as the person's overall health and age. Infected men might experience urethral irritation and swelling, along with a characteristic discharge. Infected women can also experience irritation and swelling (sometimes referred to as "strawberry cervix"), as well as a frothy discharge. This discharge can bee used for examination and diagnosis.

This is one of the least glaringly gross pictures I could find. The especially disturbing ones will simply be in the form of hyperlinks.

http://www2a.cdc.gov/stdtraining/self-study/images/vaginitis/vag-s5.gif

If you would like to look at the gross ones...here they are:
http://healthinformationfamily.com/health365days/wp-content/uploads/2011/05/trichomonass.jpg
http://reveal4real.org/images/STDs/trich.png
http://www.google.com/imgres?start=102&num=10&hl=en&safe=off&gbv=2&biw=1440&bih=799&tbm=isch&tbnid=KUxXwqHyydwXoM:&imgrefurl=http://www.consultantlive.com/sexually-transmitted-diseases/content/article/10162/34856&docid=QBbz-p3c99zY7M&imgurl=http://imaging.cmpmedica.com/consultantlive/images/articles/2002/08012002/0208ConPCUStd3F2.jpg&w=400&h=262&ei=5QZFT8jJHOTX0QHA2uyEBA&zoom=1&iact=hc&vpx=175&vpy=224&dur=6521&hovh=182&hovw=278&tx=119&ty=117&sig=116419919040292482809&sqi=2&page=4&tbnh=140&tbnw=187&ndsp=35&ved=0CKwCEK0DMEc4Hw

Though trichomoniasis can be treated with antibiotics, the disease is still dangerous. Pregnant mothers who carry the disease can be vulnerable to early-onset birth, which of course can result in many complications in the health and development of the child. Furthermore, as the parasite typically resides in the mother's vagina, the child risks infection as well. The CDC estimates that 124,000 pregnant women are infected with trichomoniasis every year, making it the fourth most common STD in pregnant women (http://www.cdc.gov/std/pregnancy/STDFact-Pregnancy.htm).

Furthermore, the swelling and irritation caused by trichomoniasis can lead to an increased probability of infection with HIV/AIDS. HIV/AIDS is of course a very prevalent global health concern. This increased susceptibility shows just how dangerous this sexually transmitted parasite can be, and indeed shows how this parasite can alter society. Though this disease is easily treated, failure or inability to do so can increase the risk to spread a much more deadly disease.

Sources:
The Center for Disease Control and Prevention
http://www.cdc.gov/std/trichomonas/STDFact-Trichomoniasis.htm

http://trichomonasvaginalis.org/

The World Health Organization

Michigan State District of Natural Resources

Brugia malayi: Agent of Lymphatic Filariasis

2012-02-22T09:52:00.000-05:00

Introduction

Brugia malayi is one of three nematodes that cause lymphatic filariasis. Lymphatic filariasis is neglected tropical disease that is most easily recognized by the symptom elephantiasis. This symptom is the swelling of the lower extremities.[5] B. malayi is only found in south and southeast Asia. The parasite is transmitted by a mosquito vector and humans are its definitive host.

Symbiont Description

Brugia malayi are long, thread-like roundworms. Male worms are capable of growing to 2cm length while females can grow up to 8cm in length when they reach the adult stage.[3]

Host Description

B. malayi reaches sexual maturation in the definitive host which can be human, monkey, domestic cats, or forest carnivores. The parasite is transmitted to the definitive host by the species of Mansonia, Aedes, Anopleles, and Culex mosquitoes. While the mosquito is taking its blood meal the larvae enter the wound.[2]

Life Cycle

http://dpd.cdc.gov/DPDx/images/ParasiteImages/A-F/Filariasis/B_malayi_LifeCycle.gif

B. malayi larvae are transmitted to a definitive host by a mosquito vector. The larvae develop into adults in the lymphatic tissue. The adults produce microfilariae that enter the bloodstream and are taken up by a mosquito vector. The cycle continues again with transmission to another host.[4]

Ecology

B. malayi is a causative agent for lymphatic filariasis. The nematodes nest in the lymph nodes stretching them until lymph fluid can only drain downward. This causes excessive pain and swelling. Both of these symptoms can be treated but there is currently no cure for filariasis. The World Health Organization hopes to eradicate the disease through the use of deworming drugs.[1]

Example of a vector-borne transmission

B. malayi is transmitted by a mosquito vector, specifically the mosquitoes of the genera Mansonia, Aedes, Anopleles, and Culex. These mosquitoes are found in the swamps and irrigated fields of Asia. The parasite resides in the stomach, thorax muscles, and the proboscis of the mosquito until it is transmitted to the definitive host.[2]

References

1. http://www.nytimes.com/2006/04/09/world/americas/09lymph.html?ex=1160884800&en=f67aded46f031e62&ei=5070

2. http://eol.org/pages/2921743/details#ecology

3. http://www.ncbi.nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?mode=Info&id=6279

4. http://dpd.cdc.gov/DPDx/HTML/Frames/A-F/Filariasis/body_Filariasis_b_malayi.htm

5. http://www.who.int/mediacentre/factsheets/fs102/en/

Babesii microti: the Protozoan Plasmodium

2012-02-21T10:25:00.000-05:00

Introduction

http://dpd.cdc.gov/dpdx/html/Frames/A-F/Babesiosis/body_Babesiosis_mic1.htm

Babesii microtiare piroplasms (protozoan parasites) that present with malaria-like symptoms inhumans. Babesiosis is the diseaseprocess of the parasite in humans, and is commonly reported in the northeasternUnited States [2]. With the protozoanusing erythrocytes as a platform for budding, symptoms such as fatigue, aches,and/or nausea and vomiting appear much like that of malaria. Through a tick vector, infected humans arealso introduced to Lyme disease and ehrlichiosis at the same time, creatingdifficulty for a proper diagnosis.

Description

Babesii is thegenus name for this protozoan. For humanparasitism, microti is the genus ofthe parasite. The symptoms presented inhumans are similar to that of malaria (Plasmodium) [1], and is oftenmisdiagnosed for this reason. Witha one to four week incubation timeinside humans, symptoms of other tick born diseases like Lyme disease may occuraround the same time, further preventing a definite diagnosis. Babesiimicroti attack red blood cells, reproduce through binary fission, anddestroy the erythrocyte when reproduction is complete. Weakness brought on by the destruction of redblood cells occurs. Some individualsinfected will have minor to no symptoms of infection. High risk patients, such as those who areimmunosuppressed, splenectomized, and/or elderly present with moresymptoms. In severe cases, patients aregiven an exchange transfusion [2].

Host's description

The white footed mouse,Peromyscus leucopus, is one of the two hosts of Babesii microti. A commonmouse, the white footed mouse is native to North America, and is found fromNova Scotia to Texas and even Mexico [4]. The deer tick, Ixodes scapularis,is the other host of Babesii microti,and is identified as the definitive host for this protozoan. The deer tick is also known for carrying Lymedisease and human granulocytic ehrlichiosis. Often times, humans who are infected with Babesii microti are also infected with Lyme disease and HEG [3]. This causes difficulty in diagnosing theinfected patient who has symptoms that can only be explained as multipleinfections.

Life cycle

http://www.dpd.cdc.gov/dpdx/images/ParasiteImages/A-F/Babesiosis/Babesia_LifeCycle.gif

Beginning with an infected tick, the sporozoites of Babesii microti enter the white-footedmouse. In the blood stream, thesporophytes enter red blood cells and reproduce through budding. This destroys the erythrocyte, and the protozoan'seventually differentiate into male and female gametes [1]. The mouse continues its life, and, whenexposed to ticks that are not yet infected, the parasite travels into the tickas its definitive host. Through contactin the mouse's bloodstream, the parasites will become sporozoites though thesporgonic cycle. The cycle will continuein this manner. However, humans can beinfected through an infected tick feeding on the human. For the parasite to enter the human throughthe tick vector, the tick has to be attached to the human for about twenty-fourhours before the parasite is passed into the human [2]. Normally, this is a dead end for theparasite. If the infected human were todonate blood and have this blood enter a non-infected human through a bloodtransfusion, the parasite may be passed on to a different individual.

Ecology

"Life Cycle ofBabesia Microti." YouTube. URI's Center For Vector-Borne Disease,University of Rhode Island, 28 July 2009. Web. 20 Feb. 2012.<http://www.youtube.com/watch?v=JOakxoorjoQ>.

Documented cases of babesiosisoccur mainly in the southern New England states near the coast. Specifically, documented cases are commonlyfound in southern New York, Wisconsin, and Minnesota [3]. Ticks are born on the ground, usually in leaflitter. With the white footed mouse alsolocated close to the ground, ticks easily find the mammal and become infectedwith Babesii microti should the mousebe infected before this contact.

Example of a shortened life cycle:

Babesii microtihave a shorter life cycle than that of other parasites. With a life cycle of two hosts, humansexcluded, the protozoan's progeny is created more quickly than that of aparasite with three hosts or more. Theearly maturation of Babesii microtiin the white-footed mouse allows for sexual reproduction to occur in the deertick, and have the sporozoites be transmitted to a mouse that is notinfected.

References

1) "Babesiosis." DPDx Laboratory Identification of Parasitesof Public Health Concern. CDC, 05 Dec. 2008. Web. 20 Feb. 2012.<http://www.dpd.cdc.gov/dpdx/HTML/Babesiosis.htm>.
2) "Babesiosis." NationalInstitute of Allergy and Infectious Diseases Home Page. NIH, 31 July 2008.Web. 20 Feb. 2012.<http://www.niaid.nih.gov/topics/babesiosis/Pages/default.aspx>.
3) "Atovaquone and Azithromycin for theTreatment of Babesiosis". Peter J.Krause, M.D., Timothy Lepore, M.D., Vijay K. Sikand, M.D., Joseph Gadbaw, Jr.,M.D., Georgine Burke, Ph.D., Sam R. Telford, Sc.D., Peter Brassard, M.D., DianePearl, M.D., Jaber Azlanzadeh, Ph.D., Diane Christianson, R.N., Debra McGrath,R.N., and Andrew Spielman, Sc.D. N Engl J Med 2000;343:1454-1458 November16, 2000. http://www.nejm.org/doi/full/10.1056/NEJM200011163432004#t=articleBackground
4) Linzey, A.V., Matson, J. &Timm, R. 2008. "Peromyscus leucopus". In: IUCN 2011. IUCN RedList of Threatened Species. Version 2011.2. <www.iucnredlist.org>.Downloaded on 20 February 2012.

Digital:
-http://www.dpd.cdc.gov/dpdx/images/ParasiteImages/A-F/Babesiosis/Babesia_LifeCycle.gif
-http://dpd.cdc.gov/dpdx/html/Frames/A-F/Babesiosis/body_Babesiosis_mic1.htm
-"Life Cycle of Babesia Microti." YouTube. URI's Center ForVector-Borne Disease, University of Rhode Island, 28 July 2009. Web. 20 Feb.2012. <http://www.youtube.com/watch?v=JOakxoorjoQ>.

Niphanda fusca: Raised by Ants

2012-02-20T14:03:00.004-05:00

https://encrypted-tbn2.google.com/images?q=tbn:ANd9GcSkjYZz5lpNanxEah68AncuYD8Ol3hDyx1I-Q4N8ousMlOaRIKn

Introduction: Niphanda fusca are a species of parasitic butterflies. As caterpillars, they steal nutritional resources from a species of ant known as Camponotus japonicas. They first enter the ant’s nest and elicit parental care from the worker ants by secreting chemicals that mimic that of the Campontus japonicas. The caterpillars continue to be fed by the ants in the nest until pupation. [1]

Symbiont Description: The Niphanda fusca are members of Phylum Arthropoda, Class Insecta, Order Lepidoptera, and Family Lycaenidae. Generally small, they have wings colored blue, red, or orange. As an adult most gather nector from flowers or feed on honeydew from aphids. The eggs are laid on leaves of the flowers, and the resulting caterpillar is slug shaped. [2]

Host Description: Camponotus japonicas are Japanese mongynous carpenter ants. Niphanda fusca are host-specific for this particular species of ant. [3] The chemical secretions that elicit parental care are only compatible with the Camponotus japonicas. The caterpillars are completely reliant on the ants for protection and nutrition until pupation. [1] Without the ants, the caterpillars would not survive, and the species would risk extinction unless it adapted another way to gain resources.

Life cycle: Niphanda fusca feed on aphid honeydew in the earliest stages of their lives. This is different from many Lycaenidae who feed on plants. [1]The larvae emit a secretion from their endocrine glands. This secretion causes the ant to carry the larva back to the nest where it continues to care for it through winter. [1] In order to ensure care from the worker ants, the caterpillar secretes chemicals that mimic that of the male carpenter ants. [3] Research has also shown that the secretion emitted by the larvae, a mixture of glycine and glucose, creates a reward for the host ant and reinforces the continuous feeding by the worker ants. [1] Both of these mechanisms allow the N. fusca to gain as much care as the ant larvae as well avoid a host attack while inside the nest. The Niphanda fusca continue to gain nutrition from the ants until pupation. Pupation occurs after hibernation during the winter months, and the N. fusca pupae close in spring. [1] An average of 10 months is spent in the ant nest. [1]

http://i.livescience.com/images/i/15063/i02/caterpillar-ant.jpg

Ecology: The reliance by N. fusca on the ant for protection and nutrition is not a strange occurrence. Most members of the family Lycaenidae have a dependent relationship with ants. [2] The secretion of amino acids by the larvae could be a way to mimic the ant larvae that take in protein from workers and release free amino acids back out to the nest for use, the amino acids secreted by the Niphanda fusca can be used as a source of nitrogen for the worker ants who feed the larvae. [1]

An example of host manipulation by a parasite: The parasitic relationship between Niphanda fusca and the ants is characterized by manipulation. The parasitic larvae secrete chemicals that elicit a change in behavior in the worker ants. The worker ants care for and feed the parasitic larvae as often as their own young.

[1] Wada, Ayako, Isobe, Yu , Yamaguchi, Susumu, Yamaoka, Ryohei, and Ozaki, Mamiko. “Taste-enhancing Effects of Glycine on the Sweetness of Glucose”. Chem. Senses (2001) 26 (8): 983-992. Oxford Journals Chemical Senses. Web. 15 Feb. 2012.
< http://chemse.oxfordjournals.org/content/26/8/983.full >.

[2] “Niphanda fusca”. Zipcodezoo, 31 Jan. 2012. Web. 15 Feb 2012. < http://zipcodezoo.com/Animals/N/Niphanda_fusca/>.

[3] Hojo , Masaru K., Wada-Katsumata, Ayako, Akino, Toshiharu, Yamaguchi, Susumu, Ozaki, Mamiko, and Yamaoka, Ryohei. “Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae).” Proc. R. Soc. B (2009) 276, 551-558. The Proceeding Royal Society Biological Sciences.Web. 15 Feb. 2012. < http://rspb.royalsocietypublishing.org/content/276/1656/551.full.pdf>.