VERY weird.
However, I doubt OS4 supports dual graphic cards.
In fact, I'd be surprised if it even supported dual monitors on one HD4650.
Both P96 (OS4) and CGX (MorphOS) support mutible (different) GFX-cards well since Zorro-time. None supports spanning (1 screen over 2 monitors) or the 2nd VGA/DVI of any GFX-card.
Another issue is OpenFirmware/UBoot/whatever as those will normally only init 1 card while the P96/CGX drivers for the PCI/AGP-cards might expect them to be initialized.
Successfully tested and an AGP-Radeon9000 + Voodoo3-PCI (normal PC version, but doesn't matter as CGX will take that card "raw") in my QuickSilver under MorphOS2.7.
Similar options should exist for OS4.