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Bloody and brutal, Hunter Hunter is a hard-hitting survivalist thriller that ratchets its tension with precision.Read critic reviews

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HUNTER HUNTER follows a family living in the remote wilderness earning a living as fur trappers. Joseph Mersault (Devon Sawa), his wife Anne (Camille Sullivan), and their daughter Renée (Summer H. Howell) struggle to make ends meet and think their traps are being hunted by the return of a rogue wolf. Determined to catch the predator in the act, Joseph leaves his family behind to track the wolf. Anne and Renée grow increasingly anxious during Joseph’s prolonged absence and struggle to survive without him. When they hear a strange noise outside their cabin, Anne hopes it is Joseph but instead finds a man named Lou (Nick Stahl), who has been severely injured and left for dead. The longer Lou stays and Joseph is away, the more paranoid Anne becomes, and the idea of a mysterious predator in the woods slowly becomes a threat much closer to home.

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Kingdom of Predators Meme


Kingdom of Predators is a theme song from the 2011 anime adaptation of Hunter X Hunter. In early 2020, the theme began to be used as background music in meme videos for its dramatic nature. Starting in June 2020, the theme was often paired with the Wait, It’s All Ohio? Always Has Been meme.


The Kingdom of Predators theme comes from the Chimera Ant arc in Hunter X Hunter, which began on April 23rd, 2013 and ended on July 2nd, 2014. The theme was used in dramatic sequences several times throughout the arc. Credited to Japanese composer Yoshihisa Hirano, the Kingdom of Predators theme was officially released on July 24th, 2013 on the Hunter × Hunter (2011) Original Soundtrack 3.YouTube user DMPlace uploaded the theme to YouTube on August 4th, 2013, where it received over 3,200,000 views in just under seven years (shown below).


On February 10th, 2014, YouTube user Leon – Music Videos used the Kingdom of Predators theme in an anime music video (AMV) that gained over 26,000 views in six years (shown below, left). On July 28th, another AMV set the theme by the same user received over 170,000 views in just under six years (shown below, right).

2020 Resurgence

On January 19th, 2020, Twitter user @LunaTheCloud used the theme in a fail video from Super Smash Brothers Ultimate with the characters Cloud Strife and Dr. Mario. The video gained over 59,000 views, 5,300 likes, and 1,000 retweets in just under seven months.

On March 6th, iFunny user Ctenophore posted a video using the theme gained over 19,000 smiles in five months (shown below). In the video, a man flips a pancake and falls onto a coffee table.

On April 3rd, Instagram user buzz_lighthole used the theme as music in a Fail compilation ending with the Coffin Dancers, gaining over 55,000 views in four months. iFunny user Can_i_touch_ur_wenus reposted the video to iFunny on the same day while crediting buzz_lighthole, gaining over 43,000 smiles in the same period.

Wait, It’s All Ohio? Always Has Been

Starting in June 2020, the Kingdom of Predators theme began to be used with the Wait, It’s All Ohio? Always Has Been meme for dramatic effect.

An early example is from a June 8th TikTok by user thatguatemalan in which the Kingdom of Predators theme is used with the "Always Has Been" meme (shown below, left). The TikTok gained over a million views and 260,000 likes in a month. On June 10th, TikTok user rydog813 used the same sound for a similar video and received over 870,000 views and 180,000 likes (shown below, right).

On June 29th, content creator largetrap combined Always Has Been and Kingdom of Predators with Rango (2011), gaining over 120,000 views on YouTube in two weeks (shown below, left). YouTuber Lessons In Meme Culture uploaded a video on July 3rd in which he noted the Kingdom of Predators theme’s use with "Always Has Been" (shown below, right).

Various Examples

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Hunter x Hunter: The 10 Best Episodes Of The Chimera Ant Arc (According To IMDb)

“Just wait until the Chimera Ant arc.” So much of the reboot for Hunter x Hunter was predicated on that line. Since fans had witnessed so many of the manga’s stories already, what everyone was looking forward to was the adaptation of the most brutal story arc in Togashi’s magnum opus.

RELATED: 10 Things You Might Not Know About Hunter x Hunter's Hisoka

To the creators’ credit, this storyline delivered. Focusing on a new species of insect which had found its way into the autonomous NGL country, the protagonists found themselves once again taking a backseat to the larger world storyline. Togashi asked the question of how humanity would deal in a world where they not only were no longer the Apex Predator, but they couldn’t simply rely on their intelligence to take the lead once again. Everything about the Chimera Ant story was fantastic, and this list talks about the best episodes, as rated by IMDb.


People should’ve been aware of what type of story Hunter x Hunter’s Chimera Ant arc was going to be long before now, but if they weren’t, 'The Strong and the Weak' certainly made things clear.

After several episodes of build-up, the new Chimera Ant King has finally emerged, and he is positively ruthless. He wastes no time establishing the new hierarchy, brutally murdering anyone who doesn’t follow his commands exactly to the letter. Meanwhile, the rest of the world has to figure out how they’re going to deal with this new Apex Predator.


More often than not, when a shonen series moves on and into a new arc, the old arc is rarely ever referenced again. Perhaps they mention how the hero is affected, and certainly, the hero will be stronger, but the characters from that arc are effectively “forgotten." Hunter x Hunter doesn’t do that, which is why 'Carnage and Devastation' stands out.

We see the main villains from the prior arc show that there’s no sorting algorithm of evil here and they have no problem wiping out a large portion of Chimera Ants that have overrun Meteor City. It’s a brutal fight, fitting for amoral antagonists.

8 GUNGI AND KOMUGI - Score 8.6

This feels like such a random episode, but it becomes key to much of the events that happen in the later episodes. Komugi is a helpless young girl who’s talented at only one thing: a game called Gungi, this universe’s version of Shogi or Chess. Mereum, out of a desire to test his mental abilities, winds up having Komugi brought to him for the purpose of defeating her, only to find he can’t.

RELATED: Hunter x Hunter: Top 10 Strongest Specialists Type Nen Users, Ranked

Togashi begins to humanize Meruem here, as the character considers simply eating Komugi, but instead winds up protecting her when she gets attacked. This episode shows the bond of a powerful friendship being born, though we know it can only end in tragedy.


The latter half of the Chimera Ant arc is something truly special. We’ve seen Hunter x Hunter’s version of Cell in Meruem, but finally, we get to see its version of Master Roshi take the battlefield.

Netero isn’t just a leader of the Hunter Organization, he's also one of the most powerful men that’s ever lived. And while he’s much older than he was at his peak, the matchup between him and Meruem is still intense. It doesn’t feel like he has a chance and yet Meruem can’t seem to keep up with Netero’s movements.


Occurring in the first third of this arc, 'Light and Darkness' reminds us that this series isn’t like any other shonen anime. Here, Kite brings Killua and Gon into the NGL as they look for the Chimera Ants, only for things to go terribly wrong.

After being noticed by one of the top Chimera Ants, Kite forces Gon and Killua to abandon him. In any other series, Kite would have survived, making it back to the two and helping to train them. Here? He becomes another victim of a group that has become increasingly more impossible to stop.


This episode has all the epic moments a viewer could possibly want. While it’s one thing to see Shoot go up against one of Meruem’s Royal Guard members and basically panic, fortunately, that’s not the whole of this episode. Humanity strikes back in full here, as Netero decides to work with Zeno Zoldyck to really kick off a proper war against the Chimera Ants.

As Zeno rains down dragons to destroy the palace, the rest of the gang struggle against the guardian of Meruem’s location, Menthuthuyoupi. Even the last scene sends chills down a viewer’s spine, with the two most powerful beings in the Hunter x Hunter universe barely noticing an enraged Meurem walk right past them.


Everything about the invasion part of this arc is so perfect, so meticulously planned it feels more like Togashi was chronicling the story of what actually happened, rather than merely making up a story.

RELATED: 5 Anime That Ended Before The Manga (& 5 That Outlived The Manga)

This episode begins that invasion storyline, but not before giving us the history of Chairman Netero. A story unlike most, Togashi gives us all the detail we need to understand just how hard this character had to work to become as powerful as he is. It feels superfluous, but after seeing the Chimera Ant King for so many episodes, this feels necessary to set Netero up as a worthwhile opponent, while getting us to become invested in his story.


One of the marks of a great writer is the ability to make one feel sympathy for even the most irredeemable characters. Make no mistake, Mereum is just that. He’s introduced by killing a pair of farmers, then murdering their child to eat its brain. But after being poisoned by Netero’s radiation, he spends his last moments with Komugi, the one human he was able to make a proper emotional connection with.

Togashi’s ability to create this without relying on romantic tension is incredible, and by the end it’s hard not to feel for them both - two souls that couldn’t be more different, spending their final moments together.

2 ANGER AND LIGHT - Score 9.7

Everything about this episode is such a beautiful subversion of shonen tropes. In most shonen series, you expect the lead character to beat the lead villain. Not so here.

Gon’s goal is beating Neferpitou, the being that killed his mentor. In most action series, a transformation is a good thing, a way to tap into the power within. That happens here as well, but it’s not “good” - rather, it’s Gon giving into the rage and hatred in his heart, creating a special Nen ability that he pays for, terribly, later. But here, it leads him to a crushing victory over Pitou; quite literally, as he beats Pitou’s face in until their skull cracks.

1 ZERO AND ROSE - Score 9.8

The highest-rated episode in the series, 'Zero and Rose' finishes off the battle between Netero and Mereum. The two of them have reached something of a stalemate, but it’s only a temporary one. Gradually, things start to swing in the favor of the Chimera Ant King, who has youth and superior strength on his side.

What makes Togashi such a great writer is how he’ll take otherwise irrelevant plot points and bring them back. Here the King’s time playing Gungi with his friend Komugi makes him into a better strategist, allowing him to survive long enough to take the win against Netero. Well, at least in combat. In reality, Netero shows Meruem the true “strength” of humankind; it’s ingenuity and willingness to go to even the darkest ends to take victory for themselves.

NEXT: 10 Things You Didn't Know About Hunter x Hunter's Ging Freecss


Next10 Anime Characters Who Took The Fall To Save Someone Else

About The Author
Sage Ashford (991 Articles Published)

Staff Writer for CBR, Sage Ashford has also written for Comicon as well as other sites such as The Gamer, and has been doing freelance work since 2014, and been working for CBR since 2017. His focus is primarily on spreading the word on obscure anime, comic books, and games whenever possible. Follow him on Twitter @ sageshinigami, or on Twitch @ sageshinigami.

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Gon, Killua and Nobunaga vs Uvogin Legendary Fight! [Hunter x Hunter]

No impact of transgenic cry1C rice on the rove beetle Paederus fuscipes, a generalist predator of brown planthopper Nilaparvata lugens


T1C-19 is newly developed transgenic rice active against lepidopteran pests and expresses a synthesized cry1C gene driven by the maize ubiquitin promoter. The brown planthopper, Nilaparvata lugens, is a major non-target pest of rice and the rove beetle (Paederus fuscipes) is a generalist predator of N. lugens nymphs. As P. fuscipes may be exposed to the Cry1C protein through preying on N. lugens, it is essential to assess the potential effects of transgenic cry1C rice on this predator. In this study, two experiments (a direct feeding experiment and a tritrophic experiment) were conducted to evaluate the ecological risk of cry1C rice to P. fuscipes. No significant negative effects were observed in the development, survival, female ratio and body weight of P. fuscipes in both treatments of direct exposure to elevated doses of Cry1C protein and prey-mediated exposure to realistic doses of the protein. This indicated that cry1C rice had no detrimental effects on P. fuscipes. This work represents the first study of an assessment continuum for the effects of transgenic cry1C rice on P. fuscipes. Use of the rove beetle as an indicator species to assess potential effects of genetically modified crops on non-target arthropods is feasible.


Rice (Oryza sativa L.) is one of the most important staple foods in the world. More than 50% of the world population (or more than 3 billion people) depend on rice for their daily lives1. The annual total planting area for rice was 29.4 million hectares in China for 2006 and China produced 29% of the world’s rice2,3. However, rice in China suffers from many insect pests, including planthoppers, Nilaparvata lugens (Stål), Sogatella furcifera (Horváth) and Laodelphax striatellus (Fallen); rice borers, Chilo suppressalis (Walker) and Tryporyza incertulas (Walker). In some regions, the water weevil Lissorhoptrus oryzophilus Kuschel, the gall midge Orseolia oryzae (Wood-Mason) and the thrip Chloethrips oryzae (Wil.) also heavily infest rice4.

To meet demands for feeding its growing population and replacing the intense utilization of insecticides in controlling pests, China has devoted great efforts to develop insect-resistant genetically modified (GM) rice lines5,6. Although no GM rice line has yet been commercialized, many transgenic lines expressing Bt proteins against lepidopteran pests, for example those expressing cry1Ab, cry1Ac, cry2Aa, cry1Fa and cry1Ca have been developed and these exhibit high resistance against lepidopteran target pestss7,8,9. To avoid potential risks to the environment associated with cultivating GM plants, any new GM plant needs to undergo a rigorous environmental risk assessment prior to its approval for commercial cultivation. An important part of this assessment, especially in the case of insect-resistant GM plants, is the evaluation of potential effects on valued non-target organisms6,10.

The brown planthopper (BPH), Nilaparvata lugens, is the important herbivorous insect of rice by sucking the phloem sap and causes huge yield loss11,12,13. It lives in rice paddies and is a significant aggressive predator of N. lugens14. It lives in the rice paddy and is recognized as a significant aggressive predator of N. lugens15. Since P. fuscipes is likely to be exposed to Cry proteins in rice fields by preying on N. lugens, the potential effects of transgenic Bt rice on this non-target natural predator should be evaluated case-by-case prior to the commercialization of transgenic Bt rice.

The Bt rice line T1C-19 expresses Cry1C protein and shows high resistance against rice leaf folder, Cnaphalocrocis medinalis Guenee16. Based on the risk assessment guidelines for insect-resistant GM crops, impacts of transgenic cry1C rice on non-target predators have already been evaluated. Laboratory studies indicated that larvae and adults of Chrysoperla subpiraticus (Neuroptera: Chrysopidae) are not sensitive to Cry1C proteins when provided in artificial diets or Bt rice pollen17. Chrysoperla sinica is a prevalent predator species in Chinese rice fields, its larvae may consume planthoppers and its adults feed primarily on pollen, honeydew and nectar18. High dosage of Cry1C proteins in the artificial diet had no detrimental impacts on the life-table parameters of Propylaea japonica (Coleoptera: Coccinellidae) and hence the growing of transgenic cry1C rice should pose a negligible risk to P. japonica19. P. japonica is a common and abundant predator in rice paddy, both the larvae and adults consume thrips, eggs and young larvae of Lepidoptera and the adults also feed on rice pollen20,21. Cry1C had no significant adverse effects on the population dynamics of arthropod predators13,22. However, there are no reports concerning impacts of Cry1C on P. fuscipes.

In this study, a tritrophic bioassay was conducted to assess whether T1C-19 plants had prey-mediated effects on the life-table parameters of P. fuscipes, when P. fuscipes preyed on N. lugens nymphs fed on T1C-19. The biotransfer of Cry1C protein expressed in T1C-19 rice to N. lugens and its subsequent transfer to P. fuscipes was investigated. To further verify whether Cry1C protein had any direct toxicity to P. fuscipes, a Tier-1 bioassay was performed in which P. fuscipes adults were fed an artificial diet incorporating purified Cry1C protein at a level much higher than that likely to be encountered under field conditions. Also, this study was to explore whether Cry1C protein could be transferred to P. fuscipes through BPH by Enzyme-linked immunosorbent assay (ELISA).


Effects of prey sources on the survival and development of P. fuscipes

The whole preimaginal development of P. fuscipes fed N. lugens nymphs was 28.9 d (Table 1). When incorporated with Drosophila melanogaster adults, the first instar, second instar, pupa and whole preimaginal durations were significantly shortened (P < 0.05) (Table 1). However, the preimaginal survival rate, sex ratio and female and male weight were not significantly affected by prey source (P > 0.05) (Table 1). The results showed that the food combination containing N. lugens nymphs added with D. melanogaster adults could shorten preimaginal stage duration of P. fuscipes.

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Impact of different artificial feeding system on development of P. fuscipes

Compared to P. fuscipes larvae fed the artificial diet only, the larval survival rate increased from 52.0 to 68.0% (P = 0.046) when their artificial diet incorporated nymphs of N. lugens (Table 2). The first and second instar larvae, pre-pupa and whole preimaginal durations were significantly shortened (P < 0.05) and the female body weight increased significantly (P < 0.05) (Table 2). When not provided with the artificial diet, a group of 45 P. fuscipes larvae all died within 6 d, indicating that they could not survive by feeding only on humus of soil. The results showed that if P. fuscipes larvae developed into adults, they must have consumed the artificial diet, which could then be used as a medium to deliver Bt protein into P. fuscipes.

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Life-table parameters of P. fuscipes fed on transgenic cry1C rice

There were no significant differences in preimaginal developmental time, preimaginal survival, female ratio, pre-oviposition, total fecundity and fresh body weight between P. fuscipes reared with first to third instar nymphs of brown planthopper fed on transgenic cry1C rice compared with non-Bt rice (P > 0.05) (Table 3).

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Cry1C protein detection in rice plants, larvae of N. lugens and P. fuscipes

ELISA assay showed that the concentration of Cry1C protein in rice sheaths was 1.8 ± 0.09 μg/g fresh weight. When first to third instar nymphs of N. lugens were reared on Bt rice, the Cry1C protein concentration in nymphs was 1.1 ± 0.0 ng/g. When P. fuscipes larvae preyed on first to third instar N. lugens nymphs fed on T1C-19, no Cry1C protein was detected in newly emerged P. fuscipes adults (Fig. 1).

Concentrations (Mean ± SE) of Cry1C in T1C-19 rice sheath, nymphs of N. lugens and larvae of P. fuscipes.

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Purified Cry1C protein bioassay and life-table parameters of P. fuscipes

The Cry1C concentrations in the artificial diets were 12.4 ± 0.9 and 11.5 ± 0.1 μg/g, respectively, before and after exposure to P. fuscipes for 24 h. No significant differences were observed in the Cry1C concentration in diets (the Cry1C concentration decreased by 7.2%) before and after exposure (Student’s t-test, P = 0.422). This indicated that Cry1C concentration was stable in the artificial diets throughout the feeding process.

The LC50 (concentration resulting in 50% mortality) of this batch of Cry1C for Plodia interpunctella larvae was 0.03 μg/g fresh weight. Before and after exposure to P. fuscipes for 24 h, the mortalities of C. medinalis larvae were 55.6% and 48.9%, respectively, fed on the artificial diets with 50 μg/g Cry1C potein. However, the mortality of C. medinalis larvae was 17.8% after feeding on the pure artificial diet. The results suggested that the artificial diets with Cry1C protein had insecticidal activity for P. fuscipes.

Significantly lower survival rate was observed in P. fuscipes fed on artificial diet containing 1 mg/g potassium arsenate (PA) relative to the pure artificial diet (P < 0.001, Fig. 2). No significant difference (P = 0.729, χ2 = 0.1210, d.f. = 1) was detected in the larval survival rate of P. fuscipes fed an artificial diet containing 50 μg/g Cry1C protein compared with pure artificial diet (Table 4). Similarly, no differences were found in the developmental duration, preimaginal survival rate and female ratio of P. fuscipes with high dosage of Cry1C compared to the pure artificial diet (Table 4).

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Survival of larvae of P. fuscipes feeding on artificial diet or artificial diet containing Cry1C/PA (50 μg/g Cry1C or 1 mg/g PA) (N = 75).

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Rove beetle (P. fuscipes) is widely distributed in all temperate and tropical continents23. It lives in humid habitats such as marshes, edges of freshwater lakes and streams and rice fields14,24. It preys on soft-bodied insect pests such as aphids, whitefly, mites, maggots of fruit fly and leaf hoppers of different crops25. Both the larvae and adults of P. fuscipes forage for food on the foliage or among tillers of rice plants26. They are important predators in rice fields and effective biological control agents against N. lugens, which is the most important pest in tropical rice fields and the main non-target insect pest in Bt rice fields27. Bt protein could expose the predator P. fuscipes insects through predation of the non-target herbivores N. lugens. Therefore, P. fuscipes is a good surrogate for non-target arthropods (NTAs) and it is vital to evaluate the effects of Bt rice on P. fuscipes prior to any commercialization. There are few reports on safety evaluation of Bt crops on P. fuscipes. There was no impact on the survival and predation function of adult P. fuscipes fed N. lugens reared with transgenic cry1Ac/cry1Ab rice in laboratory studies28; and the Cry1Ab protein expressed by maize hybrid MON810 did not influence the overall community structure of the rove beetle in a field experiment29.

Romeis et al.10 and Yu et al.30 descried the ecological risk assessment of transgenic plant for NTAs. In the present study, the ecological risk of transgenic cry1C rice to P. fuscipes was developed by two experiments: (1) a direct feeding experiment, in which P. fuscipes was fed an artificial diet containing Cry1C at a dose 10 times that it may encounter in realistic field conditions; and (2) a tritrophic experiment, in which the Cry1C protein was delivered to P. fuscipes indirectly through preying on N. lugens nymphs. The transgenic cry1C rice and Cry1C protein had no significant detrimental effects on the developmental time, preimaginal survival, female ratio and body weight of P. fuscipes. This is the first report of an assessment continuum for the effects of transgenic cry1C rice on P. fuscipes.

“Tier-1 assays” is the initial step to determine the potential hazard or toxicity of the insecticidal compound produced by GE plants, such as a Cry protein, to selected test species31. In the present study, a direct feeding experiment was carried that purified Cry1C protein was fed to P. fuscipes larvae by reference to the method of Zhou32. We selected artificial diets combining nymphs of N. lugens to deliver Cry1C protein into P. fuscipes. The oral poison potassium arsenate (PA), as a positive control, was used to verify the dietary exposure assay. This experiment showed that significantly lower survival was found in P. fuscipes fed on artificial diet containing 1 mg/ml PA relative to those fed on pure artificial diet, which indicated the test system in this experiment could be used to detect the dietary effects of insecticidal compounds potassium arsenate. No negative effect was found in the life-table parameters of P. fuscipes when provided with the artificial diet containing Cry1C at a concentration 10 times that for actual exposure concentration in the field compared with the pure artificial diet (negative control). Our experiment was the first report to evaluate the potential toxicity effect of Cry1C on P. fuscipes by use of “Tier-1 assays”.

The present study showed that different prey sources affected development of P. fuscipes. The experiment started with 50 P. fuscipes larvae when fed on N. lugens. To ensure enough prey samples, 80 P. fuscipes larvae fed on N. lugens added D. melanogaster as a supplement. The results showed that feeding P. fuscipes with both N. lugens nymphs and D. melanogaster adults significantly shortened growth duration, compared to feeding P. fuscipes with only N. lugens nymphs. This is consistent with Bong’s findings that survival and adult fecundity of P. fuscipes were negatively affected when lobster cockroach Nauphoeta cinerea (Olivier) was used as the only food resource33. Many reports have also shown that different nutritional composition of prey may alter biological parameters of predators34,35,36,37.

Brown planthopper is the important non-target herbivore in transgenic Bt rice. It piercing and sucking phloem of rice. Bt proteins of transgenic rice could be transferred to it via feeding38. However, whether Bt protein could be transferred to predators of brown planthopper are controversial. Cry1Ab and Cry2A could be transferred to Cyrtorhinus lividipennis and Hylyphantes graminicola by predation on brown planthopper fed on transgenic Bt rice39,40. While Cry2A protein could not be transferred to C. sinica and C. lividipennis via preying N. lugens fed on transgenic Bt rice38. In the current study, Cry1C also could not be transferred to P. fuscipes via predation of N. lugens. Even different predators preying N. lugens fed on the same transgenic Bt rice containing different concentration of Bt protein in the body. Further study should be focused on whether this difference is caused by the different feeding behavior of predator.

Our study was the first to elaborate the effects of transgenic cry1C rice on P. fuscipes, a predator in rice ecosystems and utilized a Tier-1 examination system and tritrophic bioassay. The results indicated that P. fuscipes was not sensitive to Cry1C protein and transgenic cry1C rice (T1C-19) poses a negligible risk to N. lugens.

Materials and Methods

Plant materials

The transgenic rice line, T1C-19 and its corresponding non-transformed parental rice Minghui 63 were used for the experiments. T1C-19 expresses a gene encoding synthetic cry1C under the control of the corn ubiquitin promoter and exhibits high resistance to stem borers and leaffolders16. Both rice lines were obtained from National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University (Wuhan, China). The culture methods of both rice lines for the laboratory experiments were described by Han et al.38 and Yoshida et al.41.

N. lugens and P. fuscipes

The original adults of N. lugens were randomly collected from paddy fields in Wuhan, Hubei Province, China. Prior to the tritrophic bioassay, N. lugens were reared on T1C-19 and Minghui 63, respectively, for more than ten generations to obtain uniform colonies. N. lugens was fed on 15-day-old rice seedlings cultured with Yoshida solution in plastic tanks.

The original individuals of P. fuscipes were also randomly collected from paddy fields in Xiaogan city. Both artificial diets and N. lugens nymphs were supplied to P. fuscipes larvae as their food source and maintained in the laboratory for more than one generation. The larvae were reared in plastic containers (22 cm length × 7 cm width × 7 cm height) covered with nylon mesh on the open end. First, a piece of wetted sponge was placed at the bottom of the container to maintain humidity, then the container was filled up to 2–2.5 cm with soil (damp soil rich in humus for raising maize) to provide a natural environment. There were 30–50 rice seedlings put into the container to feed N. lugens nymphs (100–300 first–third instar) and the roots of rice seedlings were supplied with moist cotton to maintain moisture. Meanwhile, artificial diets were put on a glass slide that was placed on the soil. In each container, 20–50 larvae of P. fuscipes were reared. The artificial diet was refreshed daily and at least 100 nymphs of N. lugens were supplied into each container daily. The artificial diet was prepared as described by Zhou32 with some modification. Liver powder purchased from Nutritional Food Co. Ltd., Yi Wei, China, Product Code: 1047457832 (specification: 3.5 g × 15 package; nutrient content: pork liver 50%, chicken liver 20%, goose liver 15%, jujube 10% and galacto-oligosaccharides 5%) and honey (acacia honey from Kangsi farmers, net 450 g, Huazhong Agricultural University) were mixed at the ratio of 5:1 and stirred with a glass rod for 1 min or more.

Newly-eclosed adults were picked out with a brush and reared in a glass beaker. The P. fuscipes adults were supplied with both N. lugens nymphs and with artificial diets. Into a 100-mL glass beaker, 200 rice seedlings were placed and reared with Yoshida culture solution and 200–400 N. lugens nymphs were raised on the rice seedlings. Then, this glass beaker was placed inside a 2000-mL glass beaker (with a piece of wetted sponge at the bottom to maintain humidity), as also was a glass Petri dish (5 cm diameter × 5 cm height) holding the artificial diet. The females laid eggs on sponge and rice seedlings. After 5 days of oviposition, the sponge and rice seedlings were transferred to a plastic container (22 cm length × 7 cm width × 7 cm height), with wetted tampons to maintain humidity. When larvae hatched, they were transferred to a plastic container for larvae rearing as described previously. All the insects were cultured and all experiments were conducted in a climatic chamber at 28 ± 1 °C, relative humidity 70 ± 5% and a light/dark cycle of 14/10 h.

Effects of prey sources on survival and development of P. fuscipes

Because P. fuscipes is a polyphagous predator in rice fields, before we conducted the prey-mediated effects of transgenic cry1C rice on P. fuscipes, it was essential to evaluate the effects of a single prey source on survival and development of P. fuscipes. If the single prey source had negative impacts on P. fuscipes, then another prey source should be added to minimize the negative effects. Therefore, two kinds of prey were supplied to P. fuscipes. Newly hatched larvae of P. fuscipes (<24 h) were put individually into glass tubes (2 cm diameter × 12 cm length) sheathe with nylon mesh. In order to maintain humidity, each glass tube was filled with a piece of wetted sponge in the bottom: (i) 9–10 nymphs of N. lugens (first–third instar), reared on TN1 rice plants, were used daily as the prey of P. fuscipes; (ii) in addition to 9–10 N. lugens nymphs daily, two adults of D. melanogaster (supplying one adult of D. melanogaster at 2 d after P. fuscipes neonates hatched, 2d at second-instar larvae of P. fuscipes, respectively) were also employed as prey of P. fuscipes. The survival and ecdysis of insects were recorded daily. Sex and body weight of rove beetle were recorded after P. fuscipes adults were emerged.

Effects of different artificial rearing system on the survival and development of P. fuscipes

Newly hatched larvae (<48 h) of P. fuscipes were individually reared in Petri dishes (5 cm diameter × 5 cm height) to evaluate whether the artificial diets met the growth and development demands of P. fuscipes and whether the P. fuscipes larvae could survive by only feeding on humus in soil. Each Petri dish contained damp soil rich in humus (1 cm in thickness) at the bottom and three different artificial rearing systems were constructed: (i) damp soil only; (ii) damp soil and artificial diet; and (iii) damp soil and artificial diet plus nymphs of N. lugens (supplying 10 nymphs of N. lugens at 6, 7 and 8 d after P. fuscipes feeding artificial diets, respectively). The survival and ecdysis of insects were recorded daily. Sex and body weight of rove beetle were recorded after P. fuscipes adults were emerged.

Effects of Bt-rice on the life-table parameters of P. fuscipes fed on N. lugens nymphs

Newly molted first instar larvae (<24 h) of P. fuscipes were put individually into glass tubes (2 cm diameter × 12 cm height) covered with nylon mesh. In order to maintain humidity, each glass tube was filled with a piece of wetted sponge in the bottom. One 15-d-old rice seedling was introduced into the glass tube as food for 9–10 (first–third instar) nymphs of N. lugens. Therefore, P. fuscipes larvae could prey on N. lugens nymphs. The rice seedlings and nymphs of N. lugens were changed daily. Two adults of D. melanogaster (supplying one adult of D. melanogaster at 2 d after P. fuscipes neonates hatched, 2 d at second-instar larvae of P. fuscipes respectively) were also employed as prey of P. fuscipes. The survival and ecdysis of P. fuscipes nymphs were monitored every day. The sex and body weight of P. fuscipes adults were recorded upon emergence of adults. For each rice line, 80 larvae of P. fuscipes were tested. Upon early emergence of the P. fuscipes, male and female were paired and reared in in a plastic petri dish (9cm in diameter) that contained a moist filter paper and was supplied 15 adults of N. lugens fed on transgenic cry1C rice daily. Moist cotton was introduced into petri dish and provided as the water supply and oviposition site. Then every dish was covered with parafilm sealed edge and small hole left unsealed for breathing. Egg number of each pair was recorded daily. Ten pairs were tested for each rice line. One moist cotton was put into each well of 24-well tissue culture plate for maintaining humidity. Eggs were collected with a brush and were put individually into each well. Egg hatching was observed every day and recorded. Thirty eggs for one replicate and three replicates for each rice line.

Cry1C detection in rice plants, N. lugens and P. fuscipes

The sheaths of 15-d-old rice seedlings, nymphs of brown planthopper (first to third instar) fed on T1C-19 or Minghui 63 and newly emerged adults of P. fuscipes that preyed on first to third instar N. lugens nymphs were collected for detection of the Cry protein. For each treatment, five samples of rice sheaths (20 mg per sample), three samples of N. lugens (approximate 35 mg per sample) and three samples of P. fuscipes adults (approximate 35 mg per sample) were tested. The methods of Cry protein contents were determined by Han et al.38.

Exposure of P. fuscipes to high dose of Cry1C

Lyophilized Cry1C protein was purchased from the Biochemistry Department Laboratory, School of Medicine, Case Western Reserve University, USA. The methods of purifying and lyophilizing Cry protein were described by Han et al.38.

P. fuscipes were reared on the artificial diet containing Cry1C protein. Three different dietary treatments were delivered to the first instar nymphs of P. fuscipes: (i) A pure artificial diet (negative control) and 30 (first–third instar) nymphs of N. lugens (respectively supplying 10 nymphs of N. lugens at 6, 7 and 8 d after P. fuscipes were fed artificial diets); (ii) An artificial diet containing 50 μg/g of Cry1C and 30 nymphs (first to third instar) of N. lugens (respectively supplying 10 nymphs of N. lugens at 6, 7 and 8 d after P. fuscipes were fed artificial diets); (iii) An artificial diet containing 1 mg/g of potassium arsenate (PA, positive control) and 30 nymphs (first to third instar) of N. lugens (respectively supplying 10 nymphs of N. lugens at 6, 7 and 8 d after P. fuscipes were fed). Three different diets were refreshed daily. Simultaneously, survival and molting of P. fuscipes were recorded daily. Sex and body weights of P. fuscipes were recorded when the adults were emerged. For each treatment, 75 P. fuscipes larvae were evaluated.

The artificial diet mixed with Cry1C was fed to P. interpunctella to determine Cry1C bioactivity on lepidopteran insects. Each bioassay included six concentrations of Cry1C (0, 0.02, 0.05, 0.08, 0.11 and 0.14 μg/g). For each concentration there were 40 newly hatched P. interpunctella larvae introduced on the artificial diets and 5 replicates were tested. After one week, the mortality of the larvae was recorded. The LC50 of this batch of Cry1C protein was measured.

In order to ensure the stability and the bioactivity of Cry1C protein of artificial diets that taken from the freezer and from diets that had been exposed to C. medinalis for 24 h, the Cry1C proteins were extracted from artificial diets and the methods described by Han et al.38. After 2 h of air-drying, fifteen Bt-susceptible first-instar C. medinalis were used in each treatment. And each treatment was three replicates. Mortality of the insects was calculated after 48 hours.

Data analysis

In all bioassays with P. fuscipes, statistical comparisons were made between each treatment and the control (pure diet). Student’s t-tests were used to compare the data of body weight. Mann–Whitney U-test was used to analyze the developmental time of nymphal. The parameters of preimaginal survival and female ratio were used by the Chi-square test. And the percentage data were arcsine–square root and transformed by SQRT (χ + 1) or log 10 (χ + 1). The effect of Cry1C protein dietary treatments on P. fuscipes survival was analyzed with the Kaplan-Meier procedure and log-rank test. All statistical analyses were conducted by the software package SPSS (version 16.0 for Windows, 2007).

Additional Information

How to cite this article: Meng, J. et al. No impact of transgenic cry1C rice on the rove beetle Paederus fuscipes, a generalist predator of brown planthopper Nilaparvata lugens. Sci. Rep.6, 30303; doi: 10.1038/srep30303 (2016).


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We thank Prof. Yongjun Lin (National Key Laboratory of Crop Genetic Improvement at Huazhong Agricultural University) for providing the transgenic rice seeds. This research was supported by the National Genetically Modified Organisms Breeding Major Project: Technology of Environmental Risk Assessment on Transgenic Rice (2016ZX08011-001).

Author information


  1. College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China

    Jiarong Meng, Juma Ibrahim Mabubu, Yu Han, Yueping He, Jing Zhao, Hongxia Hua, Yanni Feng & Gang Wu


H.X.H. designed research. J.R.M. performed the experiments. I.J., G.W. and H.X.H. wrote the manuscript. Y.N.F. raised the insects. Y.H., J.Z. and Y.P.H. analyzed the data. All authors read and approved the final manuscript.

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Meng, J., Mabubu, J., Han, Y. et al. No impact of transgenic cry1C rice on the rove beetle Paederus fuscipes, a generalist predator of brown planthopper Nilaparvata lugens. Sci Rep6, 30303 (2016). https://doi.org/10.1038/srep30303

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