@Ruthine My Hunter Legend 40.5 is a 1994.
Each of your tanks has its own separate vent line. One or more may be plugged. They way our boats are set up. two of the tanks (the forward and the aft tanks are above the top of the belly tanks so if all the valves are open, you will have a small static pressure on the belly tanks and if any of the screws holding the belly tank top on are leaking, they will continue to leak as long as there is water in either the forward or aft tank.
When you fill the belly tanks till water comes out the vent you'd be surprised at the amount of static pressure there is. If you have the sole taken off over the belly tanks you can actually see the top of the tank "bow up", hence my suggestion when you fill the belly tanks you immediately run some water out of the tanks. As to whether you use only one tank at a time that is up to you, but to minimize pressure on the belly tank cover I'd recommend you leave the belly tanks isolated unless you are using them.