- "Circus bugs?! How can you be circus bugs?!"
- —Flik, finding out that the warrior bugs aren't who he thought they were
Flik first sees them in the city after they were fired by P.T. Flea, when his "Flaming Death" act went wrong, doing a Robin Hood act, believing them to be warriors, and they believe him to be a talent scout, and he convinces them to come to Ant Island to help him deal with the grasshoppers. They soon discover their misunderstandings, and are grumpy with Flik for not telling them about actually combating grasshoppers, and attempt to leave, but after a bird attacks them, during which they save Dot, and Francis's leg is broken, they decide to stay. After hearing that even Hopper fears birds, Flik proposes creating a model bird to scare him and his gang, with the circus troupe taking credit for the idea.
Later, P.T. comes to Ant Island looking for his troupe, and inadverently reveals the truth about them. The Queen and Princess Atta banish them from the island, along with Flik as punishment for lying to the colony, however this was a fatal mistake; they put themselves in danger. When Hopper and his gang return and take over the island, Dot eavesdrops on a couple of grasshoppers discussing Hopper's scheme to squish the queen in order to discourage opposition from the ants and follows Flik and the troupe to tell them about the dire situation. Flik is still ashamed of himself for being a screw-up all the time, but some encouragement from Dot and the troupe makes him feel better and motivated to return and stop Hopper. The circus bugs present themselves to Hopper, claiming that Princess Atta invited them as a surprise for his arrival; Hopper initally orders his gang to kill them, but after seeing Tuck and Roll fight, he decides they can use a little entertainment and spares their lives. The circus bugs continue their show until Manny takes the queen for a magic trick, making Hopper demand to know where she is. At that moment, Flik and the blueberries launch the fake bird they constructed to scare the grasshoppers; it works, until P.T. sets it on fire, revealing it to be a hoax.
After seeing Thumper beat up Flik and hearing Hopper insult the colony and his troupe, P.T. realizes his mistake and teams up with the ants to defeat Hopper and his gang, resulting in Hopper getting killed by the real bird, putting his reign of terror and insult on the ant colony and troupe to an end and indicating that Hopper, not the colony and the troupe, was the real mindless soil shoving loser. Following Hopper's defeat, P.T. and his troupe spend the winter on Ant Island before returning to the circus in the spring after a brief celebration, bringing a group of acrobatic ants and Hopper's younger brother Molt (now called "Tiny" and working as a strongman) with them, while promising to come back and visit in the future and receiving a fond farewell from the colony.
- P.T. Flea: Ringmaster
- Francis: Clown
- Slim: Clown
- Heimlich: Clown
- Dim: Lion/Ferocious Beast
- Rosie: Lion Tamer
- Tuck and Roll: Human Cannonballs
- Manny: Magician
- Gypsy: Manny's Lovely Assistant
- Molt ("Tiny"): Strongman
- Ants (about 8): Acrobats
- Fireflies: Lighting, Snacks, Setup
- Spider: Musician
- Millipedes: Travel