The B24 chromosome in the Torrox population of the grasshopper Eyprepocnemis plorans is recurrently attached to a nucleolus in diplotene cells, indicating the activity of its distally located ribosomal DNA (rDNA). The frequency of males expressing the B chromosome nucleolus organizer region (B-NOR) almost doubled in 4 years. The likelihood of expressing the B-NOR increased with the B number and, in males expressing it, about 20% of their cells showed a nucleolus attached to the B. When active, the B-NOR contributed more than 25% of total cell nucleolar area (NA). Within males expressing the B-NOR, total cell NA did not differ between cells showing the active or inactive B-NOR, suggesting that total cell NA is tightly regulated in this species. However, this parameter tended to increase in this population from 1999 to 2004, in parallel to the neutralization process which is taking place in this population. Finally, an analysis of A chromosome NOR interdependence for activity revealed a positive correlation among autosomes but a negative correlation between autosomes and the X chromosome, the manifestation of which depends on B-NOR activity. These results are discussed in the context of the nucleolus as a sensor of the stress caused by parasitic B chromosomes.