Previously, Stark hole-burning spectroscopy and effects of pressure at low temperature were used to determine the number of red antenna states of the cyanobacteria Synechococcus elongatus and Synechocystis PCC6803 (Hayes, J. M.; Matsuzaki, S.; Rätsep, M.; Small, G. J. J. Phys. Chem. B 2000 104, 5625. Zazubovich, V.; Matsuzaki, S.; Johnson, T. W.; Hayes, J. M.; Chitnis, P. R.; Small Chem. Phys. 2002, 275, 47). Distinct differences in linear pressure shift rates, the magnitude of the permanent dipole moment change, fΔμ, and electron−phonon coupling strength clearly show that in Synechococcus there are three red states (C708, C715, and C719), whereas in Synechocystis, there are two red states (C708 and C714). In the Stark hole-burning spectra of the lowest states of these two systems, hole splitting was not observed, only hole broadening, for excitation polarization both parallel and perpendicular to the Stark field direction. The theories of Stark hole burning predict that splitting should occur for one of the polarizations unless there is a large, random component to the induced dipole moment change, Δμind, which is not expected to be the case for pigment−protein complexes in which the orientations of pigments relative to the protein matrix are nonrandom. In this paper, Stark hole burning at higher resolution is used to reinvestigate the absence of splitting. However, even at higher resolution, no splitting is detected. This is explained by invoking large variations of the inherent dipole moment change Δμ0 of the dimer (the origin of the red-state absorption) rather than of the induced dipole moment change. These arise from a distribution of the relative orientations and separations between the components of the dimer. This distribution also results in a random component of the polarizability change tensor, Δα. The random components of Δμ0 and Δα not only obscure the Stark splitting but also cause the large inhomogeneous broadening observed for these lowest-energy red states. Temperature-dependent hole widths were also measured for C708 and C714 of Synechocystis. For C714, a T1.3 temperature dependence was observed, consistent with dephasing by the disordered protein matrix. At 708 nm, however, much higher fluences were required to saturate the absorption of the blue edge of the C714 band and then begin to burn C708. The contribution of the C708 component to the broadening was weakly temperature dependent over the range measured, 2 to 14 K. This contribution is due to energy transfer from C708 to C714, and the width measured corresponds to an energy-transfer time of 6 ps. This observation provides further proof of the existence of two red antenna states, C708 and C714.