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Howard an active part in resisting the threatened Spanish attack were refused. He was at the time without any means of livelihood, except his irregularly paid pension. The lord admiral gave him as an asylum a 'little cell at Greenwich,' and in 1591 put under his charge 'a Spanish prisoner called Don Louis, who it was expected would divulge important secrets respecting the movements of the Spanish treasure fleet.' But Howard's relations with the Spaniard soon excited suspicion, and his prospects seemed utterly ruined. He thought of retiring to ‘a grove and a prayer-book.’

On the rise of Essex to power Howard was not slow to attach himself to the new favourite. He thus came into relations with both Francis and Anthony Bacon, much to the disgust of their mother, who warned her sons to avoid him as ‘a papist and a Spaniard.’ At the same time, with characteristic adroitness, he managed to continue in good relations with Sir Robert Cecil, and through his influence was readmitted to court in 1600, when Elizabeth treated him considerately. He took no part in Essex's schemes of rebellion, although Cecil believed him to be meditating communication with the earl on his release on parole from York House in August 1600 (Corresp. of Sir R. Cecil, Camd. Soc. p. 23). After the earl's execution he took part with Cecil in a long secret correspondence with James of Scotland. Howard's letters of advice to the king are long and obscure. James called them ‘Asiatic and endless volumes.’ Following Essex's example he tried to poison James's mind against his personal enemies, chief among whom were Henry Brooke, eighth lord Cobham [q.v.], and Sir Walter Raleigh. In letters written to Cecil he made no secret of his intention, when opportunity offered, of snaring his rivals into some questionable negotiation with Spain which might be made the foundation of a charge of treason (cf. MS. Cott. Titus, c. vi. ff. 386-92;, Ralegh, ii. 436 seq.) Howard also pressed on James the desirability of adopting, when he came to the English throne, a thoroughgoing policy of toleration towards Roman catholics. These communications convinced James of his fidelity; he wrote to Howard repeatedly in familiar terms, and, as soon as Elizabeth's death was announced sent him a ruby 'out of Scotland as a token' (cf. Corresp. of James VI with Cecil and others from Hatfield MSS. ed. Bruce, Camden Soc.)

The suppleness and flattery which had done him small service in his relations with Elizabeth gave Howard a commanding position from the first in James I's court. He attended James at Theobalds, and was made a privy councillor. On 1 Jan. 1604 he became lord warden of the Cinque ports in succession to his enemy Lord Cobham [see ], and on 13 March Baron Howard of Marnhull, Dorsetshire, and Earl of Northampton. On 24 Feb. 1605 he was installed knight of the Garter, and on 29 April 1608, when Salisbury became treasurer, he was promoted to the dignified office of lord privy seal. Grants of the tower in Greenwich Park and of the bailiwick of the town were made in 1605. In 1609 the university of Oxford appointed him high steward, and in 1612 he and Prince Charles were rival candidates for the chancellorship of Cambridge University in succession to Salisbury. His wealth and learning seem to have easily secured his election; but he at once resigned on learning that the king resented the university's action. He managed, however, to convince James I that he intended no disrespect to the royal family, and at a new election he was reappointed (, Life of Bishop Williams, pt. i. p. 21;, Annals of Cambridge, iii. 47-52). When, on Salisbury's death in 1612, the treasurership was put into commission, Northampton was made one of the commissioners.

Northampton took an active part in political business, and exhibited in all his actions a stupendous want of principle. He was a commissioner for the trial of his personal enemies Sir Walter Raleigh and Lord Cobham in 1603, for that of Guy Fawkes in 1605, and of Garnett, with whose opinions he was in agreement, in 1606. His elaborate and effective speeches at the latter two trials appear in the ‘State Trials’ (i. 245, 266). He supported the convictions of all. It was rumoured afterwards that he had privately apologised to Cardinal Bellarmine for his speech at Garnett's trial, in which he powerfully attacked the papal power, and had told the cardinal that he was at heart a catholic. The retort gained very general currency, and the failure of contemporary catholic writers to denounce Northampton in their comments on the proceedings against Garnett appeared to confirm its truth. In 1612 Archbishop Abbot is said to have produced in the council-chamber a copy of Northampton's communication with Bellarmine. In the same year Northampton summoned six persons who had circulated the story before the Star-chamber on the charge of libel, and they were heavily fined. Meanwhile, in May 1604, he acted as a commissioner to treat for peace with Spain, and in the autumn of the same year accepted a Spanish pension of 1,000l. a year. In September 1604, with even greater boldness, he sat on the commission appointed