Does each source gallery need to be on a separate page?

No, each source gallery does not need to be on a separate page. You can put all separate source galleries on a single page and link to them using their Section IDs or Section Anchor IDs (if you use a Gallery section) or Block IDs (if you use a Gallery block). For more details, you can refer to this post about IDs configuration.

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What kind of content is supported by Lightboxify URLs?

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Can I use Lightboxify URLs in a lightbox-enabled gallery?